The comparative evolutionary biology of the sibling species, Drosophila melanogaster and D. simulans.

VOLUME50

THE QUARTERLY REVIEW OF BIOLOGY

JUNE 1975

THE COMPARATIVE EVOLUTIONARY BIOLOGY OF THE SIBLING SPECIES, DROSOPHILA MELANOGASTER AND D. SIMULANS BY P. A. PARSONS

Bundoora,Victoria Department of Geneticsand Human Variation,La Trobe University, 3083, Australia ABSTRACT

1. D. melanogaster and D. simulans are siblingspecies;theyare morphologically almost identicaland genetically verysimilar. Whereastheirsexual behaviorpatternsare qualitatively similar,hybrids are rarelyproducedand whentheyare, theyare sterile. notall dataarein agreement, morechromosomal, D. melanogastergenerally exhibits 2. Although thandoes D; simulans. Utilizingthisrelationship, as well enzyme,and proteinpolymorphism in theliterature, onecan argueforan associationbetween as arguments geneticvariability presented and level of ecologicalheterogeneity. This associationis foundfor two major environmental variables,temperature and lightdependence. 3. On a seasonal basis, D. melanogaster achieveslarge populationnumbersearlyin the summer,as D. simulans does in theautumn.The ratio of D. melanogaster to D. simulans andmoreimportantly, withtemperature Macroenvironmental increases withtemperature fluctuation. factorinvolvedin numericalchangeswithinthetwospecies.Both temperature is an important for resistanceto desiccation, heterogeneous speciesfromBrisbane,Queensland,are genetically withadditivegeneticeffects and directionaldominancefor resistance,whereasat Melbourne, of D. simulans is additive Victoria,D. melanogaster is similar,but thegeneticarchitecture on an only.Desiccationresistancein theD. simulans Melbournepopulationvaries cyclically annual basis but not in the otherpopulations-apparentlydifferent genotypesare selected at different timesof the year.Between-species as in (2) above, generalizations, differentially are therefore madedifficult becauseofvariationswithinspecies. 4. Fromcollections at a vineyard and maturation winecellarcoupledwithsubsequent laboratory it is clear thatan environment in whichD. melanogaster occursexclusiveof experiments, D. simulans is one of an alcohol-associated resource.On theotherhand, in certainplaces D. simulans has displacedD. melanogaster,forreasonsas yetunknown. levels 5. In the laboratory, a numberof experiments at the intraspecific and interspecific in fitness-associated stagesof thelife cycle, showdifferences traits,such as viabilityat different to interpret, oftenbeingdependent oviposition sites,and pupationsites.The resultsare difficult or levelof competition. assessing Studiesovera seriesof temperatures upon strain,temperature, to thenatural fitnessparameters formanystrainsof bothspeciesare neededbeforeextrapolation environment is possible.The sameproblemoccurswhenpopulation-cage competition experiments someoftheseexperiments between thetwospeciesareconsidered, haveshownthatcompetition although itselfis controlled bynaturalselection. 6. The differences ratherthanqualitative, between thetwospeciesare, in general,quantitative so that,withthe exceptionof alcohol,bothspeciesuse rathersimilar environmental resources. The potentialfor rapid increasesin thespringsuggeststhatbothspeciesare morer strategists In thewild, whilesome niches,such as alcohol-associated thanK strategists. can be resources, todefinetheresources usedin naturein ordertoachievea morecomplete defined,it is imperative biologyof the two species.The value of the two speciesin linking comparativeevolutionary and geneticsis onlyjust nowbeingrealizedafteroverhalfa century ofstudying behavior, ecology, themexclusively in variouslaboratory containers. 151 This content downloaded from 129.219.247.033 on October 06, 2016 16:51:25 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).


152

[VOLUME

50

INTRODUCTION

"Thereis no sharpdivisionbetweenordinaryspeciesand siblingspecies.The latterare merelynear theinvisible end of a broadspectrumof increasingly diminishingmorphological differences betweenspecies.The occurrence ofnaturalpopulations withall thegeneticand biologicalattributes ofgoodspeciesbutwithlittleorno morphological revealsthevulnerability difference ofa purelymorphological speciesconcept"(Mayr,1963).

T

simu- zie, 1972; Parsons, 1973a, review and referHE TWO species,Drosophila lans Sturtevantand D. melanogaster ences), so a general comparison of the evoluLoew, are verysimilarand theywere tionarybiologyof the twospecies is now approconfused until 1919 when Sturte- priate. Some emphasis will be placed on the behavvant distinguished between them. The only satisfactorymorphological mode of ioral and ecological factors determining the separation is based upon differences in the distributionof the species in thewild.Two main external male genitalia. The posterior process approaches have been used: (1) the study of of the genital tergiteappears like a clam-shell fliesin naturalenvironments;and (2) the study of laboratorypopulations. In the lattercase it in D. simulansand like a small hook in D. Even though the morphological is always difficultto relate results to the wild. melanogaster. differencesbetween the species are small, the Some studies combine both approaches-a two species are discrete.Where sympatric,few commendable tendencythat has been increasinterspecificcrosses have been identifiedand, ing recently (for examples, Carson, Hardy, in any case, the hybrids are sterile. In one Spieth,and Stone, 1970; references,McKenzie survey,out of 3,872 females of both species and Parsons, 1972). Another major difficulty trappedin thewild,onlytwohad been fertilized is the reliance on strainskept formany generations in the laboratory, during which time by a male of the other species (Mourad, Tantawy,and Masry, 1972) and in a population geneticchanges could well occur and be correcage withboth species onlyabout one in 20,000 lated with unexpected changes in behavior or offspringwere produced by an interspecific ecology. In fact, the "domestication"of Drocross (Barker, 1962). Hybrids usually have sophilaspecies, in the sense of changes conselowered viability and aberrant sex ratios quent upon their introductionto a Drosophila (Sturtevant,1920; Biddle, 1932; Uphoff,1949). laboratory,has been littlestudied. Even more A high degree of sexual isolation occurs in difficult is the situationwheremutantand other spite of morphologicalsimilaritiesbetween the stocks bred for special purposes are used in species and, as will be seen, this similarity comparisons between species. The problem is extendsto theirgenotypes,ecology,and behav- one of comparing closely related species for ior. Such similarities,added to the fact that a given traitwithoutany understandingof the both survivein almost identicallaboratorycul- level of intraspecificvariabilityfor that trait. Finally,extrapolationto thewild is necessarily ture systems,implythat the needs of the two species are very similar, but yet it must be complicated by the need to consider the four assumed that there are subtle differencesin stagesof the lifecycle,eggs, larvae, pupae, and resource selection and utilization(see Parsons, imagos, since environmentalfactorscould well This 1973a). Many membersof the genus, in partic- effecteach of thefourstagesdifferentially. ular thosebeing considered,have theadvantage is presumablymost importantduring the two that there is an enormous amount of genetic most active feeding stages (larva and adult). informationknown about them, although this Since each stage contributesto the next, the is less true for the non-cosmopolitan species distributionof one stage is determined by its which are more difficult to culture in the own successes and by the stages preceding it. laboratory.Even though both D. melanogaster and D. simulanscan be easily cultured in the BEHAVIORAL ISOLATION laboratory,the amount of behavioral and ecoAlthough sexual isolationis almost complete logical informationaccumulated about them is ratherrestricted.Recentlythis area has come under laboratoryconditions,the successfulD. Y x D. simulansd cross is comunder more attention(see Parsons and McKen- melanogaster H

This content downloaded from 129.219.247.033 on October 06, 2016 16:51:25 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).

JUNE

1975]

EVOLUTION

OF DROSOPHILA

153

moner than its reciprocal (Sturtevant,1929). in such recognition,since antennaless D. meFor laboratorymatings,genotypeand age are lanogasterfemales still show some degree of important.In mass cultures,more interspecific species discriminationagainstD. simulansmales matingsoccur thando withsinglepairs,perhaps (Mayr, 1950). because of facilitationamong courting males. The femalesof D. simulansare more responThen one courtshipstimulatesother males in siveto the visual aspects of the male's courtship -thesame culture to increased activityor, mul- and are less responsive to those perceived by females tiple male courtship acts in concert to reduce theirantennae than are D. melanogaster the likelihood of rejection by a given female. (Spieth and Hsu, 1950; Grossfield,1971, 1972). Furthermore, the frequency of interspecific In fact, Hardeland (1972) observed that D. hybridizationincreases as the proportion of melanogasterpreferably courts in the dark. males to females increases (Barker, 1962) Grossfield (1971, 1972) analyzed a series of Finally,Le Moli and Mainardi (1972) showed Drosophilaspecies for components of mating the effectof recent experience on sexual pref- behaviorinto threeclasses: (1) species unaffecterences between the species by comparing D. ed by darkness,e.g., D. melanogaster; (2) species melanogaster males reared in the presence of partlyinhibitedby darkness (thatis, facultative D. simulansfemalescompared withthosereared mating occurs in the dark, e.g., D. simulans); in thepresenceof D. melanogaster females.While and (3) species in which mating is completely all males preferred to court females of their inhibitedby darkness. Grossfieldconsidersthat own species, the frequency of heterospecific the only cosmopolitan species showing partial matingswas 0.75 per cent for D. melonogaster light inhibition is D. simulans,whereas the males reared in the presence of homospecific remainderof the cosmopolitan species includdo not. Grossfieldsuggested females,and 5.4 per cent for males reared in ing D. melanogaster the presence of heterospecificfemales. that the unique situation of D. simulansmay Following Bastock's (1956) studies with D. reside in itsclose relationshipto D. melanogaster, melanogaster, Manning (1959) showed that the a relationship that reflects behavioral diversexual behaviorof the two species of males can gence or characterdisplacement from it. The be readily classified into the same major ele- lack of dependence on light in class 1 implies mentsof courtship:orientation,vibration,and a broader niche than class 2 and, of course, licking,but males of D. simulanshave longer thanclass 3. In class 3 fallsome of the specialized lag periods before courtshipand longer bouts narrow-nichespecies, including some of the of simple orientation.Hence the courtshipbe- Hawaiian species for which visual cues are of havior of D. melanogaster is the more active. criticalimportance(Carson, Hardy,Spieth,and The wing display of D. simulans is mainly Stone, 1970). Y x D. When successful,the D. melanogaster is scissoring,whereas that of D. melanogaster vibration. It seems that scissoring represents simulansd cross yieldsfemalesplus rare males. a lowerlevel of sexual excitationthan vibration, The reciprocal cross yields 0 to 25% females, since with lower stimulation D. melanogaster but occasionally up to 50%, so that cultures males show more scissoring,and withincreased with 0% can be regarded as one end of a stimulationD. simulansmales show more vibra- distribution(Sturtevant,1929; Parsons, 1972). tion. There is thereforeno differencein the In all cases the hybrids are sterile. Parsons basic organizationof the sexual behaviorof the (1972) investigatedthenumberof crossesgiving two typesof males, and observable differences offspring for interspecific crosses between are quantitative. Basically, D. simulansmales strains set up from single gravid founder fehave a slowerrise to sexual excitationthan do males collected in the wild. Five strainsof each D. melanogaster males. Bennet-Clarkand Ewing species were used, and from 5 x 5 tables (1969) have shown that the wing vibrationof incorporatingall possible interspecificcombiD. melanogastermales results in a female- nations, it was found that the number of sucstimulatingsong with a pulse interval of 34 cessfulcrossesdepended primarilyon the strain msecs, while that of D. simulansis 48 msecs. of the female; to a lesser extent the strain of Females can apparently distinguish between the male, especially for D. simulans,is also these two songs with their antennae. Even so, important.It could be argued that the greater it is probable thatother structuresare involved differencebetween maternalstrainscompared This content downloaded from 129.219.247.033 on October 06, 2016 16:51:25 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).

154


withpaternalis due toa cytoplasmiceffectborne in maternalstrains. The differences between strains probably originate in differencesbetween single gravid females from which the strains were set up, inasmuch as the strainswere tested soon after introductionto the laboratory.This interpretation parallels the conclusions of other studies traits concerned withadditional D. melanogaster includingbehavioral,morphological,and physiological ones (Parsons, Hosgood, and Lee, 1967; Parsons, MacBean, and Lee, 1969). Befurthergeneticanalyses cause of hybridsterility, cannot be carried out as they can with some other sibling species (see Dobzhansky, 1951). In any case, the above results argue for variabilityin natural populations for the controlof the degree of reproductiveisolationby natural selection-as would be expected fromevidence provided by other pairs of Drosophilasibling species (Parsons, 1973a, references).

COMPARISON OF GENOMES

Both species have karyotypicallyidentical metaphase configurations: an acrocentric X chromosome,metacentricautosomes II and III, and a small chromosome IV (Patterson and Stone, 1952). More is known geneticallyabout than about D. simulans.Those D. melanogaster loci identifiedin D. simulansdemonstrateabsolute linkage group identities between these species (Sturtevant,1929). The two species are alike for the X-chromosome gene sequence. However, there is distinctlymore crossingover near the distal end of the X in D. simulans. If, as is likely,most of the linkage data were collectedat 250 C, then,as will be shown later, 250 C is more unfavorablefor D. simulansthan D. melanogaster.Plough (1917) showed that crossingoverincreases at extremesof high and and these low temperaturein D. melanogaster, higherrecombinationvalues in D. simulansmay be explained because theywere obtained in an environmentmore unfavorablefor D. simulans This factsuggeststhat than for D. melanogaster. levels of recombinationmay be similar in the optimalenvironmentsin each species,a relation which may not necessarilybe true, but is certainlyworthyof investigation. Genetic data show thatchromosome III has an inversionin D. simulansnot present in D.

[VOLUME

50

melanogaster. Chromosome II is less well understood. Sturtevant (1929) argued that the chromosome-III inversionmay not necessarily be connected with the specific distinctiveness of the twospecies, sinceothersimilarinversions occur withinthe species D. melanogaster. Horton (1939) studied the salivarychromosomes of hybridlarvae betweenthe two species and found ten clear chromosomal rearrangements involving all chromosomes. Six were inversions,five of them very short; and four of the rearrangementsinvolvedchanges of one or more bands at the free ends of certain chromosomes. In addition, there are 14 short regions in the X and II chromosomes,where synapsis is not normal. In all, as many as 24 rearrangementsmay differentiatethe two species, but only one (in the rightarm of chromosome III) involvesmanybands. A recent technique is that of quinacrine staining,whichis based on the observationthat quinacrine and nitrogen mustard derivatives have been found to stain specific sites on chromosomesin such mannerthattheseregions fluorescewith extraordinarybrilliance(Ellison and Barr, 1971). This method demonstrates consistentdifferencesbetweenspecies for both the polyteneand the mitoticchromosomes. Hubby and Throckmorton (1968) studied various sibling species pairs withinthe genus Drosophilafor enzyme and protein similarities, and found that on the average sibling pairs share proteins with identical mobility50 per cent of the time,while for a siblingand nonsiblingspecies fromthe same species group, the figurewas an average 18 per cent. D. melanogasterand D. simulansgave a figureapproximating 50 per cent. Ashburner (1969) compared the two species for the puffing activityof their polytene chromosomes, on the ground that puffingreflectspatternsof active gene loci. It was found that about 50 per cent of the puffs were similar in the two species, in general agreement with Hubby and Throckmorton (1968). In such assessments,it is relevant to stress that identityof puffing patterns or of enzymeor proteinmobilitiesdoes not necessarily mean an identityof gene function.Some amino acid substitutionswould not be reflected at these levels. Even so, the above comparisons are likely to be meaningful. As Hubby and Throckmorton (1968) have pointed out, the conclusion that siblingspecies are very similar


JUNE

1975]

EVOLUTION

155

OF DROSOPHILA

geneticallyas well as morphologicallyhad been previouslydebated by Mayr(1963). He suggested thatsiblingspecies maybe no differentfrom other kinds of species, that is, they may be qualitativelyand quantitativelyas genetically distinctfromeach otheras are morphologically distinctspecies. (In fact,Mayr believes that the high degree of morphological similaritybetween siblingspecies is a consequence of developmental homeostasisand not of genetic similarity).The available Drosophila evidence supports a correlationbetween genetic,physiological, morphological, and behavioral similarities (Parsons, 1973a, Part III for references). D. melanogaster is very frequentlychromosomally polymorphic,but D. simulanshas not been observed to deviate from strictchromosomal monomorphism (Patterson and Stone, 1952). For example, Egyptian populations studied by Mourad and Mallah (1960) showed a range of chromosomalpolymorphismsin D. melanogaster fromdifferentregions,but a complete absence of chromosomal polymorphism in D. simulans.Similarly,in Brazil, D. melanogasteraveraged 0.64 inversions per larva, while none were found in D. simulans(Freire-Maia, 1964). Some have found thatthelevelof enzyme polymorphismis higherin D. melanogaster than in D. simulans(O'Brien and Maclntyre, 1969; Berger, 1970), a conclusiondisputedby Lewontin (1973) on the basis of data of Kojima, Gillespie,and Tobari (1970). Beardmore (1970) and Long (1970) found that the greater the level of ecological heterogeneityto which a D. melanogaster population is exposed, the greater its genetic variability.Further, a higher level of geneticallycontrolled enzyme variabilityin D. willistoniwas recordedunder a fluctuating, as opposed to a constant,environment(Powell, 1971), and higher levels of variabilitywere noted in continental as compared to island populations of the same and other species (see Ayala, Powell,and Dobzhansky,1971). Overall, D. melanogasterhas the genetic architecture supportive of a broader-niched species than does D. simulans.In agreement is the greater dependence formatingin D. simulanson lighting conditions,as already discussed. This argumentmaynotbe good formoredistantlyrelated species because otherfactorsmustbe taken into account (Selander and Kaufman, 1973). The general issue of the relativeniche-breadthsof the two species will be considered below.

SPECIES DISTRIBUTIONS

Different Localities The distributionsof both species are not known in detail, even though they are both cosmopolitan. They can be regarded as "domestic" species, and so are found in or near human habitation(Dobzhansky, 1965). In temperate and cold countries these species are unable to survive winters outdoors, and are reintroduced annually from man-protected places. For example, Ives (1970) described popfromSouth Amherst, ulationsof D. melanogaster Massachusetts,where wintertemperaturesare severe; there,overwinteringprobablyoccurs in the larval form, in a continuously available heat-generating,rotten-apple pile. Colonizations of regions with climates unsuitable at certain times of the year are undoubtedly helped by modern transportation. In certaintropicalregions,these reintroductionsmay not be necessary.Dobzhansky (1965) reportedthatD. simulanscan be found in some partsof Brazil in tropicalrain forests,far from human dwellings. From this observation he argued that D. simulansmightbe nativerather than a species introduced in the neotropics. is There are two reports that D. melanogaster being replaced by D. simulans. Hoenigsberg (1968) describeda Columbian locationwhere in was about ten times as 1963, D. melanogaster commonas D. simulans,but by 1967, D. simulans This was twice as common as D. melanogaster. change may have been caused by a new road in the collecting area. A similar shift, with unknown cause, occurred near Alexandria, Egypt (Tantawy, Mourad, and Masry, 1970). In the northernUnited States,D. melanogaster tendstobe commonerthan D. simulans,whereas in the southern United States the reverse is found (Wallace, 1968). A possible explanation for this pattern is that D. melanogastercan toleratewidertemperaturefluctuationsthan D. simulans.Freire-Maia (1964) reported that in Brazil D. simulansis commonerthan D. melanogasterin colder regions. More data are needed to resolve the reason for this difference. In Australia, the few collections that have been made agree with the pattern found in the United States in that D. simulansis commoner near to the tropics(McKenzie, 1973; McKenzie and Parsons, 1974a).



156

[VOLUME

50

lans, in the late summer. This pattern is in general agreement with Patterson's(1943) rePatterson(1943) studied the Drosophilafauna sults. D. simulansfrom Queensland (Mather, 1956) and bothspecies at Alexandria University at Aldrich Farm, Texas, and suggested that D. simulansrequires warmer weather to build up Farm, Egypt (Tantawy, 1964), followthissame large population numbers,whereas D. melano- pattern. In Melbourne, during the winterand spring gaster achieves large population sizes after colder temperatures.For the twospecies, popu- months,when the numbersof D. simulansand are low, D. immigrans constitutes lation peaks occur firstin spring in D. melano- D. melanogaster gasterand in autumn in D. simulans.Fig. 1 the vast majorityof all Drosophila.The relative numerical changes of the two sibling species presents the percentages of three species, D. D. simulans,and a thirdcosmopol- over the year were greater than those of D. melanogaster, itan species, D. immigrans,trapped in Mel- immigrans. The major seasonal environmentalvariable bourne,Australia,over theperiod January1970 is temperature.Based on Australiancollections to March 1973 (McKenzie and Parsons, 1974a). and D. simulans,there D. melanogaster increasesmore rapidlyafterthe for both D. melanogaster winterseason (June-August)when the numbers is a positiveassociationof numbersof individuof both species are low. It seems thatthe period als collected with mean daily temperature asof maximum population expansion occurs for sessed on a monthlybasis (McKenzie and Parin the spring,and for D. simu- sons, 1974a). No such relationshipwas observed D. melanogaster Seasonal Variations

-

D. melanogaster

-

-------D. simulans

D. immigrans

80 LU~~~~~A Is~~~I

CL

Is~I

LU

w409

I

1 I~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~ IIs a.~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~0 a

II

%

MONTHS FIG.1.THE

PROPORTION

COLLECTED AND D. immigrans D. simulans OFD. melanogaster,

IN THE MELBOURNE POPULATION

Collections made each month from January 1970 to March 1973. Differences from 100%are attributable also collected and included in the total. (After McKenzie to small numbers of D. lativittataand D. hydei

and

Parsons,

1974a.)


JUNE

1975]

EVOLUTION

OF DROSOPHILA

157

for D. immigrans.On a monthlybasis, mean of the D. melanogaster/D. simulanscomplex. Of daily temperaturefluctuationshows a signifi- course, macroenvironmentaldifferencessuch cant positivecorrelationwithnumbersof indi- as temperature may not totally explain difviduals collected for D. melanogaster, but not ferences in numbers among species, but must for the two other species. In the hot summer be of some importance. periods therewould be an additional stressdue There is some evidence that D. melanogaster to low humidity,and indeed in the Melbourne does not oviposit at temperaturesbelow about region,there is a negativecorrelationbetween 130 C (Michelbacherand Middlekauf,1954). In humidity,and both temperatureand tempera- the cellars of the "Chateau Tahbilk" vineyard, ture fluctuation. about 100 km north of Melbourne, no larvae The relative proportion of D. melanogaster were found in the seepage from wine casks to D. simulans,season by season, had a signifi- when temperaturesbelow 14? C were recorded cant (P < 0.001) positivecorrelationwithmean (McKenzie, 1973, and unpublished). Females monthlytemperatureand with mean monthly fromthecellarovipositedwhen placed at 200 C. temperature fluctuation (Fig. 2). Therefore Neitherspecies ovipositsverymuchbelow about temperature,whetherassessed by the mean or 140 C in the laboratory,and transferfrom low its range, is importantto the relative success temperaturesto 200 C immediatelyleads to a directincrease in ovipositionrate (MacKenzie, unpublished). Indeed, without fresh mating, females that were kept gravid D. melanogaster for at 60 C will produce offspring months 6 E when theyare placed at 200 C (Anoxalabehere tJ2 ?x and Periquet, 1970). Males kept at low temperatures still have viable sperms. Possibly the springexpansion of Drosophilapopulationsmay 6 2 be the result of mating of, or ovipositingby, gravid females (or both). In both species, egg wastage is minimalduring colder periods. MatFG. 2 R ing tests in the laboratory paralleled the ovipositiontestsin showinglittlemating below 120 C (McKenzie, unpublished). Microhabitats, .1 11 13 15 17 19 21 23 E9 as refuges,may support small populations. Above, on Mean Daily Temperatbe (wC) The rapid increase of the twospecies populations in spring demonstrates their ability to utilize resources then available. Inasmuch as E populations of the two species are annually o2 reconstitutedin the spring by a small number of founder individuals, the two species fulfil the requirementsof r strategy(McArthurand Wilson, 1967). Numerical changes appear to be relatedto macroenvironmentaltemperature, whether the effect be direct, due to some temperature-relatedenvironmental resource, or indirect,due to macroenvironmentaltemperature control over microenvironmental 2 ? 4 6 8 10 14 12 variations. di

Memn Daily

Temnperature Fluctualion

FIG.2. REGRESSIONOF THE D.

(?C)

metanogasterTo D. simulans

ENVIRONMENTAL

VARIABLES

RATIO

Temperature Above,on meanmonthly below,on temperatures; mean temperaturefluctuationsfor Melbourne, The implied effectof temperature in conAustralia (afterMcKenzieand Parsons,1974a).Sexes trollingthe distributionof the two species both combined. This content downloaded from 129.219.247.033 on October 06, 2016 16:51:25 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).

158


[VOLUME

50

bylocalityand byseason has justbeen discussed. converseforCamperdown, where temperature There are laboratoryexperiments which are variabilitywas highest(McKenzie, 1973). Data relevant to the foregoing conclusions. Strains from Melbourne collections show the depenbred from single inseminated D. melanogaster dence of the relativenumbersof the two species females that were collected in the wild have on mean daily temperatureand on mean daily been found to differin respect to the ability fluctuationin temperature (see Fig. 2). The correlates with of adult flies to withstandtemperatureshocks proportion of D. melanogaster (Hosgood and Parsons, 1968), and of larvae mean daily temperature,but correlates more to withstandhigh temperaturesduring devel- stronglywith mean temperature fluctuation opment (Parsons, 1969). Genes controllingsen- (McKenzie and Parsons, 1974a). These experiments have not evaluated the to temperatureare presentin otherwild sitivity Drosophilapopulations (Ogaki and Nakashima- effecton populations of temperaturesthatfluctuateeitherdiurnallyor on a lengthierinterval. Tanaka, 1966). No such observationshave been reportedfor Beardmore and Levine (1963) found that popthat were mainD. simulans,but there are some comparisons ulations of D. pseudoobscura betweenthe two species derived fromthe same tained under fluctuatingtemperature devellocalities. Tantawy and Mallah (1961) tested oped more genetic and developmental hoand D. simulans meostasisthan those held under constanttempopulations of D. melanogaster from Uganda, an area of high temperatures. peraturewhen the same mean temperaturewas Emergence of flies from eggs was higher for maintained,and Long (1970) found a higher in fluctuatingtemperin fitnessof D. melanogaster D. simulans,compared with D. melanogaster, the 180 C to 250 C range, whereas over the atures than in constanttemperatures.In enviperiodic fluctuations, entire range studied (100 C to 310 C), D. mel- ronmentswithshort-term anogasterexhibited higher average emergence. phenotypicflexibilitymay be particularlyreleIn agreement are some data of Hosgood and vant, but it has been argued that lengthier Parsons(1966) forfourstrainsof D. melanogaster environmentaloscillations may be better acinherent and three of D. simulans,each strain derived commodated by the genetic flexibility from a single inseminatedfemale collected in in a population (Thoday, 1956). Phenotypicand the wild,and testedin the laboratoryat 29.50 C, genetic flexibilitymay interact,especially in 27.50 C, 250 C, 200 C, and 150 C. After five populations with lengthyoscillations.This ingenerations,all the strains of D. melanogaster terpretationfitsD. simulansand D. melanogaster, were growingat all temperatures,whereas the since temperaturevariationsare both diurnal three D. simulansstrains kept at 200 C were and seasonal in the United States and in Australia.The niche of D. simulansis narrower growing,but only one of those held at 250 C in the laboratory for light-dependence and (and it died out by the 24th generation). Thus D. simulansis more restrictedin its tolerance fitness under constanttemperature than the This finding is in niche of D. melanogaster. to temperaturethan D. melanogaster. D. simulansmight thereforebe expected to accordance withcertaintheorieswhichcorrelate in regions where geneticheterogeneitywithecological heterogeoutnumber D. melanogaster temperature fluctuationsare small. Data for neity (see above). Extrapolation to natural the United States fitthisexpectationfairlywell conditions is difficult,as always, but for tem(Wallace, 1968), since D. simulansis the more perature such data as exist afford agreement common species in the southern states,where between observationsin the laboratoryand in theclimateis moreequable throughoutthe year, nature. is more common in the and D. melanogaster north,wherewintersare severeand wherewide Desiccation daily fluctuationsin temperatureoccur. Because of theirsmall size, most insectshave Comparing three Australian localities, Mela high ratio of surface area to volume, and bourne, in Victoria, Camperdown about 200 km west of Melbourne, and Brisbane, in the amount of water thatcan be lost by evapoQueensland, the D. simulans:D. melanogaster ration is large compared withthe amount that ratio was found to be highest for Brisbane, can be stored, as Machado-Allison and Craig wheretemperaturevariabilityis lowest;and the (1972) stressed for mosquitoes. Intraspecific This content downloaded from 129.219.247.033 on October 06, 2016 16:51:25 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).

JUNE

1975]

EVOLUTION

OF DROSOPHILA

159

differencesin resistanceto desiccation exist in of suitableones. For each variable,populations a numberof species. For D. melanogaster, genetic in differenthabitatsshould be considered. resistancetodesiccationcan be assessed bydeath Desiccation is an easier stressthan high temrates in a desiccator. Resistantindividualstend perature to study in the laboratory.The Meltobe large and to have highwetand dryweights bourne and Brisbane populations of the two (Parsons, 1970). Levins (1969) studied the ther- species, represented by strains derived from mal. acclimation of a number of Drosophila single inseminated females, were studied for speciesin thestressenvironmentof 370 to 380 C, theirabilityto withstanddesiccation(McKenzie where heat is confounded withdesiccation. He and Parsons, 1974b). Brisbane is characterized concluded that acclimation in various species by periods of high temperaturesassociated with depended on theirgeneticheterogeneity,their high humidities,whereas Melbourne endures associated withphysi- hightemperaturescoupled withlow humidities. developmentalflexibility ological acclimation, and their behavioral Generally, D. simulans was less resistant to as is true mechanisms(habitat selection). D. melanogaster desiccationthan was D. melanogaster, showsall threemechanisms.The geneticheter- for a variety of other physiological stresses ogeneitycomponent was demonstratedby Par- (Parsons, 1973b). Heterogeneity between sons (1970). D. simulanshas poorer develop- strainswas consistentlyfound forboth species. mental flexibility and physiologicalacclimation For the Melbourne population of D. simulans, than D. melanogaster(Levins, 1969). Conse- changes in mean mortalityfollowed a cyclical quently,D. simulansdepends less on these two pattern.The population was most resistantto factorsfor acclimation.In contrast,D. simulans desiccation during the summer and became progressivelyless resistantas the weather beexhibitsgreater genetic differencesthan does from Melbourne D. melanogaster. Hence the relativeordering of came cooler. D. melanogaster the factors permittingacclimation may vary exhibited no seasonal cyclicalpattern. For the between species, and it can be argued that the Brisbane populations, bothspecies showed no D. melanogaster systemwould enable itto occupy seasonal variationin mean mortality. a widerniche thancould the D. simulanssystem, At regular intervals,these populations were at least in so far as immediate acclimation is tested for their genetic architecture by the concerned. Of the various species he studied, technique of diallel crossing (McKenzie and Levins (1969) judged D. melanogaster to possess Parsons, 1974b). Additive genetic effectswere the broadest niche, and D. simulansto possess found for both species in both localities. In a relativelynarrow niche. all populations except that of D. simulansfrom Laboratory studies on environmentalstress Melbourne,therewere nonadditiveeffectswith pay littleattentionto the mobilityof drosophi- directionaldominance forresistanceto desiccalids, a factorthat must be relevantin the wild. tion. The resultsof diallel crossingsuggest that Behavioral adaptations add a new dimension there is a similarityin genetic architecture to the capabilities of an animal, for when betweenthose populations thatmaintaina relastressed, it has the option of moving; it can tivelyconstantdesiccationmortality throughout avoid potential stress altogether by judicious the year. The D. simulans population from and alterable microhabitatselection.The envi- Melbourne, which has regular annual changes ronmentaldiversityavailable to adults is clearly in desiccation tolerance, also has a different greaterthan the environmentaldiversityavail- genetic architecturefor this tolerance. Of all able to larvae, but larvae may experience a populations of both species, when flies were considerable heterogeneity in temperature, kept at 150 C, 200 C, or 250 C in the laboratory moisture,and chemicals.Larvae can move away and were tested for desiccation mortalityover fromlethal levels of such variables. An under- a number of generations(McKenzie and Parstandingof the comparativeecology of the two sons, 1974b), only the D. simulanspopulation speciesultimately depends upon knowledge,for from Melbourne was different. Unlike the all stages of the life cycle, of the extremes at others, it exhibited a correlationbetween the which death occurs, of the conditions under temperatureand the mean mortality.Both at which there is optimal development, and the 200 C and 250 C, itsresistancewas greaterthan extentto whichbehavioralmechanismscan aid at 150 C, up to the tenthlaboratorygeneration. in avoiding unsuitable habitats or the choice When the 150 C and 250 C populations were This content downloaded from 129.219.247.033 on October 06, 2016 16:51:25 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).

160


interchangedas regards theirtemperatureenvironments,the resistance increased in the formerbut decreased in the latter population over the next five generations(generations 10 through 14 in the laboratory). The relativelyconstantmortalitiesfromdesfromMelbourne and iccationof D. melanogaster ofboth species fromBrisbane suggestthatthese populations have quite high levels of physiological and genetic homeostatis. The diallel crosses revealed interactioncomponents indicating that interactinggenes may be involved in desiccation resistance. On the other hand, the D. simulanspopulation fromMelbourne has a genetic architecturethat is almost entirely additive,and genes thatact additivelyforresistance to desiccation could change rapidly in frequency.Apparently,differentgenotypesare selected directionallyat differenttimes of the year. The Melbourne weather cycle thus leads to two different genetic architectures,both of which control desiccation resistance; in one the architecturecorrespecies, D. melanogaster, sponds to that of its Brisbane counterpart; in the other, D. simulans,it does not. The only plausible conclusion is that the Melbourne D. simulans population adapts by a mechanism differingfromthe adaptation of other populations. EthylAlcohol Preliminarycollectionsat a vineyardand its associated maturationcellar at "Chateau Tahbilk" near Melbourne showed thatboth species were present in the vineyard,whereas only D. was presentin the cellars (McKenmelanogaster zie and Parsons, 1972). This observation led to a series of laboratory experiments which demonstratedthe following. 1. Adults of D. simulansare very sensitive to media containing 6 or 9 per cent alcohol survived aftersix days, whereas D. melanogaster well (Fig. 3). 2. For mean percentagesof larvae emerging as adults in media containing the above concentrationsof alcohol, the differencesbetween species were much smaller. Overall, D. melanogasterlarvae were more tolerantof alcohol than D. simulanslarvae. 3. As judged by oviposition preferences when offered a choice of media with 0 or 9

[VOLUME

50

D. melanogaster D. simulans 100

0 100 014 U

LU50

LU

0

0 3 6 9 0 3 6 9 PERCENTAGE ALCOHOL

3. MEAN PERCENTAGE SURVIVAL OF ADULT D. melanogaster AND D. simulans AFTER Six DAYS ON 0, 3, 6, OR 9% ALCOHOL After McKenzie and Parsons, 1972.

FIG.

per cent alcohol in population cages, D. melanogasterhas a small tendencyto ovipositpreferen-

tiallyon alcohol-supplementedmedia, whereas D. simulans exhibited a highlysignificantpreference for standard medium sites (Table 1; see McKenzie and Parsons, 1972). During vintage (harvest) at "Chateau Tahbilk" fermentationtakes place in tanksdirectly above the cellars. Exclusively D. melanogaster

TABLE 1 on mediacontaining9% alcohol Numberofeggsoviposited or 0% alcoholin populationcages and D. simulanstested separately D. melanogaster (after McKenzie and Parsons, 1972). The data are summed over strains,trials,and temperatures(200 C and 25? C). D. melanogaster D. simulans

9% ALCOHOL

0% ALCOHOL

1,843

1,627 1,356

677


JUNE

1975]

EVOLUTION

OFDROSOPHILA

161

reoccupyan area once alcohol is removed from it, as was shown by collectionsof larvae from grape residues that had dried considerably. 4 . From such sitesboth species eclose. This study provides one more situationwhere D. melanogasterhas the broader niche. Because of the specificityand localization of the alcohol, ex2 trapolation from laboratoryto field and vice versa is much simplerthan it could be for the more general stressesof temperatureand de._o0 0 siccation. The presence of a resource that contains 0 20 alcohol adds an extra component of heteroge40 60 0 neity to the environment.This could lead to acgenetic differentiationin D. melanogaster, a NON cording to locality. Given sufficientenvironVINTAGE E C 1 4 PERIOD mental heterogeneityand selection pressure, genetic differentiationmay occur over rec markablyshortdistancesin plants (Antonovics, ..E Bradshaw, and Turner, 1971) and in insects (Ford, 1971). The cellar population of D. me6i 2 lanogaster larvae was significantly more resistant to alcohol than larvae that were immediately outside the cellar,and the latterpopulation was more resistantthan a Melbourne population. No such differenceswere found forD. simulans. 0 20 40 60 Assuredly,natural selectionis operating in the Distance From Fermenting Area (metres) "Chateau Tahbilk" D. melanogaster population. No correlationwiththe alcohol dehydrogenase FIG. 4. RELATION OF THE D. simulans/D. melanogaster (ADH) system appeared to exist(McKenzie and RATIO TO DISTANCE FROM THE FERMENTATION TANK DURParsons, 1974c). *

VINTAGE PERIOD

ING AND AFTER VINTAGE

AfterMcKenzie,1974.

was found at the fermentationtanks, and it was present in excess up to 20 meters from them (Fig. 4). Furtheraway, the normal vineyard excess of D. simulanswas found. From release-recaptureexperimentsduring vintage, it appears that D. melanogaster regularlymoves towards the cellar, whereas D. simulansmoves away from it (McKenzie, 1974). Thus the distributionof the two species at vintage time is apparentlya functionof their dispersal activities, in agreement with our laboratoryexperiments, which showed that the presence of alcohol in the environmentaltersthe behavioral patternof thespecies. Aftervintage,the normal excess of D. simulanswas found in the fermentationarea but not in the maturationcellar. Alcohol is thereforea resource or attractant exploited only by one of these two species. In fact,it does not take long for D. simulansto

NutritionalRequirements Erk and Sang (1966) used outbred laboratory stocks to measure larval development as an indicatorof nutritionaladequacy. They found thatrequirementsforprotein(casein), carbohydrate, fat (cholesterol),nucleic acids and vitamins were similar,but not identical, for the two sibling species. An exception was biotin to survive, whichis necessaryforD. melanogaster but the development of D. simulanswas unaffected by the presence of biotin from zero to high concentrations.In general, the requirementsof thesespecies are similar,though there are some minor differences. BEHAVIOR THROUGHOUT

THE LIFE CYCLE

Behavior can be observed at most stages of the life cycle, but few integratedstudies have been carried out. Both in pure species cultures


162


[VOLUME

50

and in competition experiments, D. simulans to changes in the kinds of yeasts(Candida puland Nadsonia elongata)collected from tends to oviposit more to the center of food cherrima oranges and bananas in the same locality as does (Moore, 1952a; cups than D. melanogaster Barker, 1971). D. simulanstendsto choose drier the flies. Studies on both laboratoryand wild ovipositionsites,and the resultsof D. simulans- yeastsshow D. simulansto be more homeostatic for yeast tolerance than D. melanogaster.In competitionexperimentscan be D. melanogaster changed by alteringthe drynessof the surface respect to fitnesson media supplemented with available foroviposition.One factor,not tested certain yeasts, D. simulansmust be regarded as havingthe broader niche. However,the story in D. simulans,is the tendency shown by D. on media is far from complete, since El-Helw and Ali to lay eggs preferentially melanogaster already in use by larvae, even those of another (1973) found differinglarval viabilities and developmentaltimesaccording to the strainof species (del Solar and Palomino, 1966). The generalityof this result should be tested by Saccharomycescerevisiae which was present. using manystrainswithina species. For examp- Clearly, yeasts are significantin determining le, Soliman (1971) described quantitativedif- the distributionand abundance of these two ferencesin ovipositingbetween D. melanogaster Drosophilaspecies. Barker (1971) found that D. simulanstends strainsfromAlexandria, Egypt,and Florida. Larvae show preferences in the laboratory to pupate directlyon the medium much more although the actual for differentparts of the available medium. than does D. melanogaster, A D. simulansvermilioneye mutant strainwas proportionsof various locations of pupation, found to go deeper into the medium than a especially in D. simulans,depended upon the yellow, white (body color, eye color) mutant number of adults. For D. simulansonly, the strain of D. melanogaster(Barker, 1971). If proportionof pupae on the medium decreased general, the D. simulanspattern could signify as larval density increased. Variables such as adaptation to a dry environment.However, an experimental technique, media, and genetic observation made by Sturtevantin 1920, that strain make comparisons of differentexperiunfavorably ments problematical. in old dryculturesD. melanogasteris affectedmore quicklythan D. simulans,was not Sameoto and Miller (1968) found that both confirmedby Moore (1952a). In relationto the species responded to a medium with a high proportion of founding adults, a higher water contentby an increase of pupae on the emerged than D. sides of vials,byan increasein the totalnumber proportionof D. melanogaster simulansin mixed cultures (Tantawy and Soli- of pupae produced, and also by an increase ceased emerging in pupal mortality;but the total number of man, 1967). D. melanogaster adults produced were not affectedby the mois22 days after the cultures were set up, and D. simulans25 days after.This differencesug- ture content of the medium. A dry medium gestsa greateradaptation of D. simulansto the produced a change in the pupation behavior conditions of old cultures, in which greater of D. simulans.Compared with early pupating concentrations of micro-organisms tend to D. simulans,which lived on a moistermedium, occur. Athighlarvaldensities,thelarvalviability late-pupating D. simulanstended more to reof D. simulansdecreased less on media supple- main on the surfaceof theirdried-outmedium. mented with Saccharomyces cerevisiaethan did No such change occurred in D. melanogaster. and D. the larval viabilityof D. melanogaster; However, caution in interpretationis necessary on simulansproved fitterthan D. melanogaster because the data were based upon examination media supplemented with Schizosaccharomycesof only one strainfromeach species. Furtherpombe(El-Helw and Ali, 1970). D. simulansmay more, genetical variation for pupation site Thus Sokal (1966) be better able to adapt to old cultures than occurs in D. melanogaster. D. melanogaster can, because of the tendency successfullyselected for eitherpupation on the of D. simulanslarvae to go lower into the med- wall of vials or for central, nonwall pupation. Furthermore, he encountered marked difium (Barker, 1971). Probablyin agreement is the observationof ferences in pupation site that were probably El-Helw, Ali, and Moawad (1972) for flies due to minor chemical differencesin media. collected near Alexandria, Egypt, that D. mel- Such resultsmay affectany generalizationsto anogasteris more sensitive than D. simulans be made. This content downloaded from 129.219.247.033 on October 06, 2016 16:51:25 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).

JUNE

1975]

EVOLUTION

OF DROSOPHILA

163

The dispersal activityof D. melanogaster ex- D. melanogaster, maximumcourtshipactivitywas ceeded that of D. simulans,especially when found to occur just before dawn (Hardeland, dispersingtowarda lightsource (McDonald and 1972). Extrapolation to a spectrum of strains Parsons, 1973). Without a light source, no withinand between species, and to a spectrum heterogeneitywas found between strainsof D. of environmentsis clearlynecessary. simulans,but with a light source, there was heterogeneity;hence the expression of genetic COMPONENTS OF FITNESS differencesbetween strainsis light-dependent. Both the dispersal activityand matingbehavior Some comparative studies of fitness traits of D. simulansare more light-dependentthan have been carried out at the intraspecificand that of D. melanogaster. Clearly,D. melanogaster interspecificlevels. Except where stated otheris the broader-nichedspecies. Along a gradient wise, all experimentsdescribed in this section of light intensities,D. simulansshowed greater were carried out at 250 C. Many of the studies positivephototaxisthan D. melanogaster, but D. were carried out with very few (and often showed a more even distribution special) strains.Therefore extreme caution is melanogaster over the various lightintensities-another sug- necessaryin extrapolatingto the species level gestion of a broader niche for D. melanogaster in view of the genetic heterogeneityfound in (Parsons, 1974). Some behaviors have not yet naturalpopulationsof Drosophilaforalmostany been compared between the two species; these measurable trait (Parsons, 1973a). Miller include geotaxis and chemotaxis, which have (1964a,b) looked at intraspecificand interspeso far been almost wholly,but not extensively, cificlarvalcompetitionforone laboratorystrain studied in D. melanogaster and D. simulans,in larvae (see Parsons, 1973a). each of D. melanogaster One complication,not fullyexplored even of uniform age at densities of 5 to 300 per in D. melanogaster, is that of cyclical changes vial containing5 cc of agar live-yeastmedium. over a 24-hour period. Many Drosophilaspecies Up to approximately160 larvae, the performtend to avoid traps except at dawn, dusk, or ances of the two species were strikingly similar. both; this behavior may be related to local Both species showed comparable changes in conditionsof temperatureand humidity.Data length of the larval period and in mortality, collected at Camperdown, 200 km west of pupal viability,numbers of adults produced, Melbourne, show this behavior for D. melano- ultimate adult body weight, and biomass of gasterand D. simulans(McKenzie, 1973). Some adults in response to changes in initial larval Hawaiian species may present an exception to density.Above a densityof 160 larvae per vial, bimodal daily activity(Carson, et al, 1970). In D. melanogaster had a higher survivalrate than D. melanogaster, the activityof neurosecretory D. simulans,since D. simulanswas then unable cells shows peaks at around dawn and dusk to extend its larval development time whereas (Rensing, 1964), as does adult oxygen con- D. melanogaster continued to lengthenits develsumption (Rensing, Brunken, and Hardeland, opment time up to a densityof 300 per vial. 1968). Rhythmsforoviposition(Gruwez,Hoste, At high larval densities,D. simulanshad a low Lints,and Lints,1972) and foreclosion (Harker, larval mortalityand a high pupal mortality.D. 1965) also exist. Harker believes that eclosion melanogaster had a higher larval mortalityand occurs primarilyat dawn because of circadian a lower pupal mortalitythan D. simulansat the rhythmsof earlier stages of development.Eclo- same densities. We immediatelysee the comsion at dawn, when the air is moist and cool, plications in any assessment of the relative so thatthewingscan be unfoldedand the cuticle successesof the two species. In fact,in interspehardened in an equable environment, must cificcompetitionexperimentslasting one gensurely minimize risks from a stress such as eration, little difference between the species desiccation.Clearly,an explorationof variations occurred at low larval densities, although at in eclosion withinand between the two species a densityof 160 larvae per vial, D. melanogaster would be of value, especially since Rensing, had a slightadvantage, which was accentuated Brunken,and Hardeland (1968) reportedsome at still higher densities. This density effect differencesin eclosion between mutant strains corresponds to that in the intraspecificdata of D. melanogaster. Not unexpectedly,circadian (Miller, 1964a,b). rhythmsmay occur for courtshipbehavior. In Sameoto and Miller (1966) recorded the This content downloaded from 129.219.247.033 on October 06, 2016 16:51:25 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).

164


number of adult offspringand the pattern of eclosion from a 10-day period of oviposition, in lines of each species selected for maximum thorax length. Single females of both species had sigmoid productivitycurves,withD. simulansproducingthe largestnumberof offspring. When the oviposition period was held to six days, and the densityof femaleswas increased, second-degree productivitycurves were obtained for both species. In thiscase, D. melanogasterproducedmoreoffspringthanD. simulans at each female density. These and other studies (e.g., Barker, 1967) indicate that factorsdeterminingproductivity and involvingvarious phases of the life cycle high show some superiorityof D. melanogasterat population densities. When attemptingto extrapolate to interspecificcompetitionin population cages, weightshould be placed on what happens under the most rigorous environmentalconditions.In population cages, D. melanogasterusually excludes D. simulansat 250 C (Moore, 1952ab; Futuyma,1970; Tantawy and Soliman, 1967); but at 15? C, the reverse may occur (Moore, 1952a; Tantawy and Soliman, 1967). This apparent dependence of fitness upon temperatureseems to have been rather overlooked, in view of the earlier evidence has a broader niche showingthatD. melanogaster than D. simulans.It would be of considerable interestto look in detailat the situationat about 200 C, where D. simulansmay show superiority. The extrapolationof laboratoryexperiments to wild populations is made even more difficult if Barker and Podger's (1970a) results are considered. They showed that the outcome of interspecificcompetitionover one generation is both frequency-dependent and densitydependent. In particular,they found that results for mixed cultures were not predictable from results acquired with single-speciescultures,especiallyat highdensities.Furthermore, Barker and Podger (1970b) showed that D. females raised in mixed cultures melanogaster were less fecund than females from pure cultures,whereas D. simulansshowed the reverse. There are thereforea number of fairlysubtle variables differentiatingthe two species and requiring careful experimentationfor detection. One problem in generalizing from the observationsby Barker and Podger, however, an Oregon-R-C strain is that in D. melanogaster was used, and in D. simulansa vermilion-eye

[VOLUME

50

mutantstrainwas employed. Caution is necessary in extrapolating from strain to species. For example in population cages at 25? C, D. simulanswas eliminated in 19 of 20 cages in about 100 days. In the twentiethcage, D. simulans remained much longer (Moore, 1952a,b). Using differentpopucompeting with an lations of D. melanogaster inbred strain of D. simulans,Futuyma (1970) studied interspecificcompetitionover ten generations at 250 C. A varietyof outcomes was observed, the explanation of which appears to require qualitativelydifferentchanges in different populations. Futuyma argues that the genetic variance of traitsused in interspecific competitionand resource utilizationis highly nonadditive.That may be expected, since competitive ability is likely to be under strong directionalselectionforhighcompetitiveability, and so would leave ratherlittleadditivegenetic variation(see Parsons, 1973a, for references). Gibo (1972) foundgreatdiversityin smallmixed and D. simulans, populations of D. melanogaster both in population size and as to the dominant species,no doubt because differingcompetitive abilitiesin the small populations reflectedgeneticdifferences.As would be expected in cages with large population sizes, the results were more uniform. This variabilityof results is consistentwith observationsof changes in interspecificcompetitive ability-frequently an increase aftercompetition (Moore, 1952a,b; Gibo, 1972; Hedrick, 1972; Barker, 1973). Thus, the interspecificcompetitiveabilitiesof the pair of species D. serrataand D. nebulosa improvedover a numberof generations(Ayala, 1969). Perhaps that result indicates that when two species compete for certain limited resources, natural selection may produce genotypes which are better competitors for that resource. It is also possible that selectioncould favor the avoidance of competition-that is, could favor genotypesexploitingresources not utilizedby the competingspecies. Selection for avoidance of competitionpresumablyincreases the probabilityof coexistence, and so leads to the ecological divergenceof two coexistingspecies. Barker (1973), experimenting with D. and D. simulans,expressed a belief melanogaster that there may be evidence for the evolution ofavoidance of competitionby means of ecological divergence.An alternativeexplanation put forwardby him was that of the evolution of


JUNE

1975]

EVOLUTION

OF DROSOPHILA

165

differences,but because of the general similarities betweenthe two species theymay be rather difficultto unravel. A recurrentthemehas been the issue of niche breadth. Generally, studies on survival at extremetemperaturesand on the relativedependence of the two species on light for mating and for dispersal activityshow that D. melanogastercan be regarded as having the broader niche, and that alcohol at a sufficientconcentrationleads to a niche occupied only by D. melanogaster. Levins (1969) concluded that, of a number of Drosophilaspecies he had studied, D. melanogaster has the broadest niche of all, and relies upon itsdevelopmentalflexibility and physiological acclimation for adaptation more than does D. simulans,which relies more on genetic differences.For example, there is a differinggenetic architectureof resistance to desiccation of the two species collected in Melbourne.On theotherhand, sincethe genetic of D. simulansdiffersbetweenMelarchitecture CONCLUSIONS bourne and Brisbane,between-speciesgeneralAndrewarthaand Birch (1954) argued per- izations can be made only with caution. Yet suasively for the natural control of insect D. simulansis a verysuccessfulspecies in many numbers by density-independentfactorssuch environments;it is favoredover D. melanogaster as climate,ratherthan by food and space. The in regions of lower temperature fluctuation. twospecies under consideration,D. melanogaster Further distributionsurveys are needed, but and D. simulans, are probablynot greatlylimited thoserecorded are in agreement.A nichewhere D. simulansmight be favored would be one by a shortageof resources. Population sizes and limitsto population growthmost likelyreflect in which it could utilize a varietyof natural the availabilityof time during the year when yeast species; furthermore,it is likely that its the rate of increase of populations of these survivalis aided by its abilityto burrow deeper can. It is imperspecies is positive.In general, the potentialfor intomedia than D. melanogaster rapid increaseby both species frompresumably ative to tryto identifythe differentresources small numbersof individualsthatsurviveover- used by the two species in nature. wintering(at leastin the Melbourne population) Finally, although these species are easy to argues thatboth species are "colonizers."They studyin the laboratory,a major unsolved probfulfillthe requirementsof r strategists,as de- lem resultsfromthe near impossibility of replifined by MacArthurand Wilson (1967). While cating the heterogeneityof the microhabitat the concepts of r and K strategiescan only found in the wild. Also, how do physiological be regarded as relative rather than absolute and behavioral mechanisms help to adapt to (Gadgil and Solbrig, 1972), the similaritiesof this heterogeneity?At this complex level, we D. melanogaster and D. simulansto each other approach the limitsimposed by the geneticand are evident. In spite of these strategicsimilari- ecologicalsuitability of the organisms.Although ties,manydifferencesbetweenthe species exist. the two species in question have been studied These differencesare primarily quantitative extensivelyin the laboratoryformanydecades, ratherthanqualitative,so thatboth species may theirvalue in helping to linkbehavior,ecology, be presumed to utilize rather similar environ- and genetics is just beginning to be realized. mental resources. One exception is the utiliza- Studies of this multidirectionalnature should tion of the alcohol-associatedresource at "Cha- contributemuch to evolutionarybiology as a teau Tahbilk" by D. melanogaster alone. Further whole. At least a starthas begun at the macroresearch may well reveal additional discrete habitatlevel, as this reviewshows.

an increase in facilitation,wherebyone or both species beneficiallyaffectsthe other. Thus, whereverstudied, the components of fitnessdifferbetweenthe twospecies,but there is also variation within species for the same components, whether examined as pure or mixed culture comparisons. For components of fitness,it is not possible to say to what extent variationat the intraspecificlevel overlaps with thatat the interspecificlevel. Another problem is thatmostof the laboratoryexperimentswere carried out at 250 C, which is a more extreme temperaturefor D. simulansthan it is for D. melanogaster. Hence, studies over a series of temperatures, fixed or fluctuating, where competitionand fitnessparametersare assessed for many strains,preferablyrecentlycollected in the wild, are essential before extrapolation to the wild can be attempted.


166

THE QUARTERLY REVIEW OF BIOLOGY ACKNOWLEDGMENTS

The Australian Research Grants Committee has supported the pertinent work performed in the

[VOLUME

50

author's laboratory. I am grateful to Lee Ehrman for her careful review of the manuscript,and to J. A. McKenzie and G. J. Prince for helpfuldiscussions.

LIST OF LITERATURE ANDREWARTHA, H. G., and L. C. BIRCH. 1954. The Distribution and AbundanceofAnimals.University of Chicago Press, Chicago. ANOXLABEHERE, D., and G. PERIQUET. 1970. Resistance des images aux basses temperatureschez Drosophila melanogaster.Bull. Soc. Zool. Fran., 95: 61-70. ANTONOVICS,J.,A. D. BRADSHAW, and R. G. TURNER. 1971. Heavy metal tolerancein plants. Adv. Ecol. Res., 7: 1-85. ASHBURNER, M. 1969. On the problem of genetic similaritybetween sibling species-puffing patterns in Drosophilamelanogaster and Drosophila simulans.Am. Natur.,103: 189-191. AYALA, F. J. 1969. Evolution of fitness.IV. Genetic evolution of interspecificcompetitiveability in Drosophila.Genetics, 61: 737-747. AYALA,F. J.,J.R. POWELL, and TH. DOBZHANSKY. 1971. Polymorphismsin continentaland island populationsof Drosophilawillistoni. Proc.Natl. Acad. Sci. U. S., 68: 2480-2483. BARKER, J. S. F. 1962. Sexual isolation between Drosophilamelanogaster and Drosophilasimulans.Am. Natur.96: 105-115. . 1967. The estimationof relativefitnessof Drosophilapopulations. V. Generation intervaland heterogeneityin competition.Evolution,21: 299309. . 1971. Ecological differencesand competitive interactionbetween Drosophilamelanogaster and Drosophilasimulansin small laboratory populations. Oecologia,8: 139-156. . 1973. Natural selectionforcoexistanceor competitiveabilityin laboratorypopulations of Drosophila.Egypt.J. Genet.Cytol.,2: 288-315. BARKER, J. S. F., and R. N. PODGER. 1970a. Interspecific competitionbetween Drosophilamelanogaster and Drosophilasimulans:effectsof larval densityon viability,developmental period and adult body weight.Ecology,51: 170-189. . 1970b. Interspecificcompetitionbe, and _ tween Drosophila melanogasterand Drosophila simulans.Effectsof larval densityand short-term adult starvationon fecundity,egg hatchability and adult viability.Ecology,51: 855-864. BASTOCK, M. 1956. A gene mutationwhich changes a behavior pattern.Evolution,10: 421-439. BEARDMORE, J. A. 1970. Ecological factors and the variabilityof gene-pools in Drosophila.In M. K. Hecht and W. C. Steere (eds.), Essaysin Evolution

and Geneticsin Honor of TheodosiusDobzhansky p. 299-314. Appleton-Century-Crofts,New York. BEARDMORE, J. A., and L. LEVINE.1963. Fitness and environmental variation. I. A study of some polymorphicpopulations of Drosophilapseudoobscura.Evolution,17: 121-129. BENNET-CLARK, H. C., and A. W. EWING.1969. Pulse intervalas a criticalparameter in the courtship song of Drosophilamelanogaster. Anim.Behav., 17: 755-759. BERGER, E. M. 1970. A comparison of gene-enzyme variationbetween Drosophilamelanogaster and D. simulans.Genetics,66: 677-683. BIDDLE, R. L. 1932. The bristlesof hybridsbetween D. melanogaster and D. simulans.Genetics,17: 153174. CARSON,H. L., D. E. HARDY, H. T. SPIETH, and W. S. STONE. 1970. The evolutionarybiology of the Hawaiian Drosophilidae. In M. K. Hecht and W. C. Steere (eds.), Essaysin Evolutionand Genetics in Honor of TheodosiusDobzhansky, p. 437-543. New York. Appleton-Century-Crofts, DEL SOLAR, E., and H. PALOMINO, 1966. Choice of Am. oviposition sites in Drosophilamelanogaster. Natur.,100: 127-133. TH. 1951. Genetics DOBZHANSKY, and theOriginofSpecies (3rd. ed., revised). Columbia UniversityPress, New York. .- 1965. Wild and domesticspecies of Drosophila. In H. G. Baker and G. L. Stebbins (eds.), The Geneticsof ColonizingSpecies,p. 533-546. Academic Press, New York. EL-HELW, M. R. and A. M. M. ALI. 1970. Competition between Drosophilamelanogaster and D. simulans on media supplemented with Saccharomyces and Schizosaccharomyces. Evolution,24: 531-537. 1973. Fitnessof Drosophilaon media ,__ and __. supplemented with differentraces of Saccharcerevisiae. omyces Egypt.J.Genet.Cytol., 2: 283-297. EL-HELW, M. R., A. M. M. ALI, and H. MOAWAD. 1972. Fitnessof Drosophilamelanogaster and D. simulans in relation to natural genera of yeasts. Egypt. J. Genet.Cytol.,1: 196-202. ELLISON, J.R., and H. J. BARR. 1971. Differencesin the quinacrine stainingof the chromosomes of a pair of siblingspecies: Drosophilamelanogaster and Drosophilasimulans.Chromosoma, 34: 424435. ERK, F. C., and J. H. SANG. 1966. The comparative


JUNE

1975]

EVOLUTION

OF DROSOPHILA

nutritionalrequirementsof two sibling species Drosophilasimulansand D. melanogaster. J. Insect. Physiol.,12: 43-51. FoRD,E. B. 1971. EcologicalGenetics(3rd. ed.). Chapman and Hall, London. FREIRE-MAIA,N. 1964. Chromosomal monomorphism in Brazilian and Argentine populations of Drosophilasimulansand Drosophilarepleta.Genetics, 50: 1447-1448. FUTUYMA,D. J. 1970. Variation in genetic response to interspecific competitionin laboratorypopulations of Drosophila.Am. Natur.,104: 239-252. GADGIL, M., and 0. T. SOLBRIG. 1972. The concept of r-and K-selection:evidence fromwild flowers and some theoreticalconsiderations.Am. Natur., 106: 14-31. GIBO, D. L. 1972. A stabilizinginteractionbetween the founder effect and interdeme mixing in competingpopulations of Drosophilamelanogaster and Drosophilasimulans.Canad. J. Zool.,50: 325331. GROSSFIELD, J. 1971. Geographic distribution and light-dependent behavior in Drosophila. Proc. Natl. Acad. Sci. U.S., 68: 2669-2673. . 1972. The use of behavioral mutantsin biological control.Behav. Genet.,2: 311-319. GRUWEZ, G., C. HosTE, C. V. LINTS,and F. A. LINTS. 1972. Oviposition rhythmin Drosophilamelanogasterand its alteration by a change in the photoperiodicity.Experientia, 27: 1414-1416. HARDELAND, R. 1972. Species differences in the diurnal of courtship behaviour within the rhythmicity melanogastergroup of the genus Drosophila.Anim. Behav.,20: 170-174. HARKER, J. E. 1965. The effectof a biological clock on the developmental rate of Drosophilapupae. J. Exp. Biol., 42: 323-337. HEDRICK,P. W. 1972. Factorsresponsiblefora change in interspecificcompetitiveabilityin Drosophila. Evolution,26: 513-522. HOENIGSBERG, H. F. 1968. An ecologicalsituationwhich produced a change in the proportion of Drosophila melanogaster to Drosophilasimulans.Am. Natur.,102: 389-390. HORTON, I. H. 1939. A comparison of the salivary gland chromosomes of Drosophila melanogaster and D. simulans.Genetics,24: 234-243. HOSGOOD, S. M. W., and P. A. PARSONS. 1966. Differencesbetween D. simulansand D. melanogaster in tolerances to laboratory temperatures. DrosophilaInformation Service,41: 176. , and __. 1968. Polymorphismin natural populations of Drosophilafor the abilityto withstand temperatureshocks. Experientia, 24: 727-728. HUBBY,J.L., and L. H. THROCKMORTON. 1968.Protein differencesin Drosophila.IV. A study of sibling species. Am. Natur.,102: 193-205. IvEs,P. T. 1970. Furthergeneticstudiesof the South

167

Amherst population of Drosophilamelanogaster. Evolution,24: 507-518. KoJIMA, K-I., J.GILLESPIE,and Y. N. TOBARI. 1970. A profileof Drosophilaspecies' enzymesassayed by electrophoresis.I. Number of alleles, heterozygosities,and linkage disequilibriumin glucosemetabolizingsystemsand some other enzymes. Biochem.Genet.,4: 627-637. LE MOLI, F., and M. MAINARDI. 1972. Effettodi esperienze recentisull' isolamentoriproduttivotra e Drosophilasimulans.IsDrosophilamelanogaster titutoLombardo(Rend. Sc.), B 106: 29-35. LEVINS,R. 1969. Thermal acclimationand heat resistance in Drosophilaspecies. Am. Natur.,103: 483499. LEWONTIN,R. C. 1973. Population genetics.Ann. Rev. Genet.,7: 1-17. LONG,T. 1970. Geneticeffectsof fluctuatingtemperature in populations of Drosophilamelanogaster. Genetics,66: 401-416. MAcARTHUR,R. H., and E. 0. WILSON. 1967. The Theory PrincetonUniversityPress, ofIslandBiogeography. Princeton. McDONALD, J.,and P. A. PARSONS. 1973. Dispersal activitiesof the siblingspecies Drosophilamelanogasterand Drosophilasimulans.Behav. Genet.,3: 293-301. McKENZIE, J. A. 1973. Studies on the ecological geneticsof Drosophila.(Ph.D. Thesis, La Trobe University). .-1974. The distributionof vineyardpopulations of Drosophilamelanogaster and Drosophilasimulans during vintage and nonvintageperiods. Oecologia, 15: 1-16. McKENZIE, J. A., and P. A. PARSONS. 1972. Alcohol tolerance:an ecological parameterin the relative success of Drosophilamelanogaster and Drosophila simulans.Oecologia,10: 373-388. and __. 1974a. Numerical changes and envi__, ronmental utilizationin natural populations of Drosophila.Aust.J. Zool.,22: 175-187. and __. 1974b. The genetic architectureof __, desiccationresistancein populationsof Drosophila and Drosophilasimulans.Aust.J. Biol. melonogaster Sci., 27: 441-456. and __. 1974c. Microdifferentiation in a natu__, ral population of Drosophilamelanogaster to alcohol in the environment.Genetics,77: 385-394. MACHADo-ALLISON,C. E., and G. B. CRAIG JR. 1972. Geographic variationin resistanceto desiccation in Aedes aegyptiand A. atropalpus(Diptera: Culicidae). Ann. Entomol.Soc. Amer.,65: 542-547. MANNING,A. 1959. The sexual behaviourof twosibling Drosophilaspecies. Behaviour,15: 123-145. MATHER,W. B. 1956. The genus Drosophila(Diptera) in eastern Queensland. II. Seasonal changes in a natural population 1952-1953. Aust. J. Zool., 4: 65-75.


168


E. 1950. The role of theantennae in the mating behaviorof female Drosophila.Evolution,4: 149154. .- 1963. Animal Species and Evolution.Harvard UniversityPress, Cambridge. MICHELBACHER, A. E., and W. W. MIDDLEKAUF. 1954. in NorthernCalifornia. Vinegarflyinvestigations J. Econ. Entomol.,47: 917-922. MILLER, R. S. 1964a. Interspeciescompetitionin laboand ratorypopulations of Drosophilamelanogaster Drosophilasimulans.Am. Natur.,98: 221-238. .-1964b. Larval competitionin Drosophilamelanogasterand D. simulans.Ecology,45: 132-148. MooRE,J. A. 1952a. Competitionbetween Drosophila and Drosophilasimulans.I. Populamelanogaster tion cage experiments.Evolution,6: 407-420. . 1952b. Competitionbetween Drosophilamelanogasterand Drosophilasimulans.II. The improvement of competitive ability through selection. Proc.Nati. Acad. Sci. U.S., 38: 813-817. A. M., and G. S. MALLAH. 1960. Chromosomal MouRAD, polymorphismin Egyptian populations of DroEvolution,14: 166-170. sophilamelanogaster. MOURAD, A. M., A. 0. TANTAWY, and A. M. MASRY. 1972. Studies on natural populations of Drosophila. XIII. Chromosomal polymorphismin and its relation to resistDrosophilamelanogaster ance to certaininsecticides.Egypt.J. Genet.Cytol. 1: 141-148. O'BRIEN, S. J.,and R. J. MACINTYRE. 1969. An analysis of gene-enzymevariabilityin natural populations and D. simulans.Am. of Drosophilamelanogaster 103: 97-113. NVatur., OGAKI, M., and E. NAKASHIMA-TANAKA. 1966. Inheritanceof radioresistancein Drosophila.I. Mutation Res.,3: 438-443. PARSONS, P. A. 1969. A correlationbetween the ability to withstandhigh temperaturesand radioresisExperientia,25: tance in Drosophilamelanogaster. 1000. .- 1970. Genetic heterogeneityin natural populations of Drosophila melanogasterfor ability to withstanddessication. Theoret.Appl. Genet.,40: 261-266. . 1972. Variations between strainsof Drosophila and D. simulansin givingoffspring melanogaster in interspecificcrosses. Can. J. Genet.Cytol.,14: 77-80. 1973a. Behavioural and Ecological Genetics:A .__ Studyin Drosophila.Clarendon Press, Oxford. .- 1973b. Geneticsof resistanceto environmental stresses in Drosophila populations. Ann. Rev. Genet.,7:239-265. .-1974. Phototacticresponses along a gradient of light intensitiesfor the sibling species DroD. simulans.Behav.Genet., sophilamelanogasterand 5:17-25. PARSONS, P. A., and J.A. MCKENZIE. 1972. The ecologi-

MAYR,

[VOLUME

50

cal geneticsof Drosophila.Evol. Biol., 5: 87-132. P. A., S. M. W. HOSGOOD, and B. T. 0. LEE. 1967. Polygenes and polymorphism.Molec.Gen. Genetics,99: 165-170. PARSONS,P. A., I. T. MAcBEAN, and B. T. 0. LEE. 1969. Polymorphismin natural populations for genes controllingradioresistancein Drosophila.Genetics, 61: 211-218. PATTERSON,J. T. 1943. The Drosophilidae of the South-west.Univ. of Texas Publ.,4313: 7-216. PATrERSON,J.T. and W. S. STONE. 1952. Evolutionin theGenusDrosophila. Macmillan,New York. PLOUGH, H. H. 1917. The effectof temperatureon crossing over in Drosophila.J. Exp. Zool., 24: 147-209. POWELL,J. R. 1971. Geneticpolymorphismsin varied environments.Science,174: 1035-1036. of corpus allatum RENSING,L. 1964. Daily rhythmicity and neurosecretorycells in Drosophilamelanogaster(Meig.). Science,144: 1586-1587. RENSING,L., W. BRUNKEN,and R. HARDELAND. 1968. On the genetics of a circadian rhythmin Dro24: 509-510. sophila.Experientia, SAMEOTO,D. D., and R. S. MILLER. 1966. Factors conof Drosophilamelanogaster trollingtheproductivity and D. simulans.Ecology,47: 695-704. 1968. Selection of pupation site by ,__ and __. and D. simulans.Ecology, Drosophilamelanogaster 49: 177-180. SELANDER,R. K., and D. W. KAUFMAN. 1973. Genic and strategiesofadaptationin animals. variability Proc.Nat. Acad. Sci. U.S., 70: 1875-1877. SoKAL, R. R. 1966. Pupation site differencesin DroUniv.Kansas ScienceBulletin, sophilamelanogaster. 46: 697-715. SOLIMAN, M. H. 1971. Selection of site of oviposition and D. simulans.Am. by Drosophilamelanogaster Midl. Natur.,86: 487-493. SPIETH, H. T., and T. C. Hsu. 1950. The influence of lighton the matingbehavior of seven species of the Drosophila melanogasterspecies group. Evolution,4: 316-325. STURTEVANT, A. H. 1919. A new species closelyresem26: 153-155. Psyche, bling Drosophilamelanogaster. .-1920. Genetic studies on D. simulans.I. IntroGenetics, duction. Hybrids with D. melanogaster. 5: 488-500. .- 1929. The genetics of Drosophila simulans. CarnegieInst. Wash.Publ.,399: 1-62. TANTAWY,A. 0. 1964. Studieson natural populations of Drosophila. III. Morphological and genetic differencesof wing lengthin Drosophilamelanogasterand D. simulans in relation to season. Evolution,81: 560-570. TANTAWY,A. O., and G. S. MALLAH. 1961. Studies on natural populations of Drosophila.I. Heat resistance and geographical variation in Drosophila and D. simulans.Evolution,15: 1-14. melanogaster

PARSONS,


JUNE

1975]

EVOLUTION

OF DROSOPHILA

A. O., and M. H. SOLIMAN. 1967. Studies on natural populations of Drosophila. VI. Competitionbetween Drosophilamelanogaster and Drosophilasimulans.Evolution,21: 34-40. TANTAWY, A. O., A. M. MouRAD,and A. M. MASRY. 1970. Studieson naturalpopulationsof Drosophila. VIII. A note on the directionalchanges over a long period of timein thestructureof Drosophila near Alexandria, Egypt. Am. Natur., 104: 105-

TANTAWY,

169

109.

J.M. 1956. Population genetics.Nature,178: 843-844. UPHOFF, D. E. 1949. The expression of alleles at the cubitus interruptuslocus in hybridsbetween D. melanogaster and D. simulans.Genetics,34: 315327. WALLACE, B. 1968. Topicsin PopulationGenetics.Norton, New York.

THODAY,


A comprehensive study of genic variation in natural populations of Drosophila melanogaster. VI. Patterns and processes of genic divergence between D. melanogaster and its sibling species, Drosophila simulans.

Relationships within the melanogaster species subgroup of the genus Drosophila (Sophophora) i. inversion polymorphisms in Drosophila melanogaster and Drosophila simulans.

D. simulans hybrids.

Intraspecific and interspecific variation at the y-ac-sc region of Drosophila simulans and Drosophila melanogaster.

Differential responses to artificial selection on oviposition site preferences in Drosophila melanogaster and D. simulans.

Adaptive evolution of genes involved in the regulation of germline stem cells in Drosophila melanogaster and D. simulans.

Comparison of lethal mutations of Drosophila melanogaster with D. simulans when detected by the attached-X method.

Alfred Henry Sturtevant and crosses between Drosophila melanogaster and Drosophila simulans.

Courtship song and mating speed in hybrids between Drosophila melanogaster and Drosophila simulans.

Genetic and Transgenic Reagents for Drosophila simulans, D. mauritiana, D. yakuba, D. santomea, and D. virilis.

The ribosomes of Drosophila. IV. Electrophoretic identify among ribosomal subunit proteins from wild type and mutant D. melanogaster and D. simulans.

Evolutionary biology and pathology of vitamin D.

Dosage compensation of the Drosophila pseudoobscura Hsp82 gene and the Drosophila melanogaster Adh gene at ectopic sites in D. melanogaster.

Genetic analysis of aspartate aminotransferase isozymes from hybrids between Drosophila melanogaster and Drosophila simulans and mutagen-induced isozyme variants.

Surface structure of the compound eye of various Drosophila species and eye mutants of Drosophila melanogaster.

The evolutionary history of Drosophila buzzatii. XXIII. High content of nonsatellite repetitive DNA in D. buzzatii and in its sibling D. koepferae.

The organization of the histone genes in Drosophila melanogaster: functional and evolutionary implications.

The ribosomes of Drosophila. III. RNA and protein homology between D. melanogaster and D. virilis.

Exploring the Phenotypic Space and the Evolutionary History of a Natural Mutation in Drosophila melanogaster.

Genetics of sexual isolation in females of the Drosophila simulans species complex.

Comparative validation of the D. melanogaster modENCODE transcriptome annotation.

Isozyme variability in species of the genus Drosophila. VIII. The alcohol dehydrogenase polymorphism in North Carolina populations of D. melanogaster.

Limited gene misregulation is exacerbated by allele-specific upregulation in lethal hybrids between Drosophila melanogaster and Drosophila simulans.

Ethanol: larval discrimination between two Drosophila sibling species.