VOLUME
50
THE QUARTERLY REVIEW OF BIOLOGY
THE EVOLUTIONARY
MARCH
1975
ORIGIN OF FEATHERS
BY PHILIP J. REGAL MuseumofNaturalHistory,University ofMinnesota,Minneapolis,Minnesota55455 ABSTRACT
Previoustheoriesrelatingtheoriginof feathersto flightor to heat conservation are considered to be inadequate.There is need for a modelof featherevolutionthatgives attentionto the to reveal functionand adaptiveadvantageof intermediate structures. The presentmodelattempts and todeal with,thespectrum ofcomplexquestionsthatmustbe considered. In severalgeneraof modernlizards,scalesare elongatedin warmclimates.It is arguedthat thesescalesact as smallshieldsto solar radiation.Experiments thattendto confirm are reported this.Using lizardsas a conceptualmodel,it is arguedthatfeathers likewisearoseas adaptations to intensesolar radiation.Elongatedscales are assumedto have subdividedintofinelybranched structures thatproduceda heat-shield, flexibleas well as long and broad. Associatedmuscles had thefunctionof allowingthe organismfine controlover ratesof heat gain and loss: the couldbe movedto allow baskingin cool weatheror protection specializedscalesor earlyfeathers in hot weather.Subdivisionof the scales also alloweda closefit betweenthe elementsof the insulativeintegument. Therewouldhave beenmechanicaland thermaladvantagestohavingbranchesthatinterlocked intoa pennaceousstructure earlyin evolution,so thefirstfeathers mayhave beenpennaceous. A versatile insulationofmovable, branched scaleswouldhavebeena preadaptation forendothermy. As birdstookto the air theyfaced coolingproblemsdespitetheirinsulativecoveringbecause of high convectiveheat loss. Shortglides may have initiallybeen advantageousin coolingan animal under heat stress,but at some point theproblemmay have shiftedfromone of heat exclusionto one of heat retention. Endothermy probablyevolvedin conjunctionwithflight.If so, it is an unnecessary assumptionto postulatethatthe climatecooledand made endothermy advantageous. The development of feathersis complexand a modelis proposedthatgives attentionto the fundamental problems ofderivinga branchedstructure witha cylindricalbasefroman elongated scale.
F
INTRODUCTION
EATHERS are a unique featurethat distinguishesthe birds from reptiles. Despite their complex construction, feathersare generallyagreed (though it is not proved) to have been derived fromscales ratherthan to have arisen de novo. Although most accounts in textbooks include some sort of speculation on the evolutionary origin of feathers,there has been surprisingly littledetailed discussion of the subject: unified treatmentof the problems involved is lacking. As one authorrecentlypointedout, "We cannot
as yet offerany plausible explanation for the originof the unique shaft,barbs, and barbules without which modern feathers would have neither aerodynamic nor insulatoryfunction" (Maderson, 1972a, p. 427). Anotherauthor has referred to "the morass of contradictory theoriesand muddy thinkingthat occurs in so much of the literatureon thissubject" (Parkes, 1966, p. 77). Broadly speaking, the chief difficultyin thinkingabout theevolutionofthe firstfeathers is the difficultyin accounting for the genesis of the structurethrougha continuoussequence of selectiveforcesand witha continuous series
35 This content downloaded from 129.219.247.033 on October 07, 2016 14:34:33 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
36
THE QUARTERLY REVIEW OF BIOLOGY
of hypotheticalmorphological steps that are functionallyplausible. I shall attemptto formulate a model of feather evolution that gives particularattentionto the need forclear identificationof selectiveforces and to the need for functionalcontinuityattending any proposed morphologicaltransition.The model, of course, is speculative,since the available fossilfeather material is scanty and is difficultto place in phylogenetic sequence with any confidence. The model is not merelyan attemptto present a scheme that will withstandtestingand criticism. It is also an attempt to define as fully as possible the range of problems that must be dealt with in considering the origin of feathers. Any comprehensive scheme for the evolutionaryorigin of feathers must address itself simultaneouslyto several questions. Prominent among these is the problem of identifyingthe selective pressures that produced the first feathers.Were the firstfeatherseffectiveprimarilyin flightor gliding,or were theyeffective primarilyin heat transfersituations?Another importantquestion concernsthe detailed architectureof the feathers.How did the branching structureof shaft,barbs, and barbules evolve? How did the systemof tinyhooks and overlapping barbules that binds the feather surface into a pennaceous web evolve? The structure is so complex that it is simply not enough to suppose thatonce the scale had become frayed and perhaps down-like,hooked barbules were somehow added to the filamentousstructures to produce a flat,strong,flexible vane, as in the modern feather (an idea implicitin some literature).Indeed, the intermediatestructure that must be envisaged when one adds hooks to the filamentsof a down-likestructurecould resultin a tangledmess, more like a briar patch than a contour feather.Such failure clearly to outline intermediatesteps in the evolution of feathersand to justifythe hypotheticalstructures in terms of their adaptive value to the individual pervades the literatureon this subject. The model to be presentedhere willbe based in large part on a considerationof lizard scales. I do not wish to imply,however, that feathers derived fromlizard scales. Birds, of course, did not evolve from lizards. They did not even evolve fromlepidosaurian reptiles.The closest livingrelativesof birds are crocodilians,if one
[VOLUME
50
accepts that the derivation of crocodilians, dinosaurs, and birds is from the Thecodontia (Bock, 1969; Brodkorb, 1971). Among living reptiles, the crocodilians are similar to birds and unlike other reptiles,not only in certain aspects of their anatomy,but also in that,like birds, they build and guard nests, guard the young after hatching (Cott, 1971), and use sounds in communicationbetween motherand young as well as between males and females. Birds and crocodilians are also unusual and similar in that stones are taken up into a muscular portion of the stomach, where they possiblyaid in digestion.So the avian gizzard, while oftenconsidered an adaptation for flight (Welty,1962), may simplyreflectthe thecodont origin of birds. It is logical to assume thatwe should examine the integumentof crocodiles and alligators to gain insightintothe originsof the avian integument. Crocodilians,however,are highlymodified for aquatic life. The integument of a crocodilianmay not offerus any special insight into the conditionof the pre-avianintegument. On the other hand, many of the lizards, such as Sceloporusand Agama, have raised leaf-like scales on their bodies, neck regions, and tails and legs (Fig. 1). The effectis verymuch like a series of overlapping shingles on a roof. In the lizards mentioned, each shingle-likescale is raised, forming an opening between the underside of the anterior scale and the top surface of the posterior scale. Other lizards, for example, skinks,have large leaf-likeoverlapping scales thatare notraised butare pressed tightlyagainst one another, exactly like the shingleson a roof. It is from a consideration of the heat transferpropertiesof large, raised scales such as those on Sceloporusthat I believe we can make some progress in understanding the evolution of feathers.These scales will be shown to functionas a heat or radiation shield. Since thermoregulationis an important present-day functionof bird feathers,and since we can demonstrateinstanceswhere the evolution of enlarged scales on reptiles is probably a result of thermal selective pressures in the environment,the relationship between these twoobservationsshould be seriouslyconsidered forwhateverlightit mayshed on the evolutionary origin of feathers. The followingessay is divided intofivemajor sections. The firstsection deals criticallywith
This content downloaded from 129.219.247.033 on October 07, 2016 14:34:33 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
1975]
MARCH
ORICIN OF FEATHERS
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50
THE QUARTERLY REVIEW OF BIOLOGY
THE EVOLUTIONARY
MARCH
1975
ORIGIN OF FEATHERS
BY PHILIP J. REGAL MuseumofNaturalHistory,University ofMinnesota,Minneapolis,Minnesota55455 ABSTRACT
Previoustheoriesrelatingtheoriginof feathersto flightor to heat conservation are considered to be inadequate.There is need for a modelof featherevolutionthatgives attentionto the to reveal functionand adaptiveadvantageof intermediate structures. The presentmodelattempts and todeal with,thespectrum ofcomplexquestionsthatmustbe considered. In severalgeneraof modernlizards,scalesare elongatedin warmclimates.It is arguedthat thesescalesact as smallshieldsto solar radiation.Experiments thattendto confirm are reported this.Using lizardsas a conceptualmodel,it is arguedthatfeathers likewisearoseas adaptations to intensesolar radiation.Elongatedscales are assumedto have subdividedintofinelybranched structures thatproduceda heat-shield, flexibleas well as long and broad. Associatedmuscles had thefunctionof allowingthe organismfine controlover ratesof heat gain and loss: the couldbe movedto allow baskingin cool weatheror protection specializedscalesor earlyfeathers in hot weather.Subdivisionof the scales also alloweda closefit betweenthe elementsof the insulativeintegument. Therewouldhave beenmechanicaland thermaladvantagestohavingbranchesthatinterlocked intoa pennaceousstructure earlyin evolution,so thefirstfeathers mayhave beenpennaceous. A versatile insulationofmovable, branched scaleswouldhavebeena preadaptation forendothermy. As birdstookto the air theyfaced coolingproblemsdespitetheirinsulativecoveringbecause of high convectiveheat loss. Shortglides may have initiallybeen advantageousin coolingan animal under heat stress,but at some point theproblemmay have shiftedfromone of heat exclusionto one of heat retention. Endothermy probablyevolvedin conjunctionwithflight.If so, it is an unnecessary assumptionto postulatethatthe climatecooledand made endothermy advantageous. The development of feathersis complexand a modelis proposedthatgives attentionto the fundamental problems ofderivinga branchedstructure witha cylindricalbasefroman elongated scale.
F
INTRODUCTION
EATHERS are a unique featurethat distinguishesthe birds from reptiles. Despite their complex construction, feathersare generallyagreed (though it is not proved) to have been derived fromscales ratherthan to have arisen de novo. Although most accounts in textbooks include some sort of speculation on the evolutionary origin of feathers,there has been surprisingly littledetailed discussion of the subject: unified treatmentof the problems involved is lacking. As one authorrecentlypointedout, "We cannot
as yet offerany plausible explanation for the originof the unique shaft,barbs, and barbules without which modern feathers would have neither aerodynamic nor insulatoryfunction" (Maderson, 1972a, p. 427). Anotherauthor has referred to "the morass of contradictory theoriesand muddy thinkingthat occurs in so much of the literatureon thissubject" (Parkes, 1966, p. 77). Broadly speaking, the chief difficultyin thinkingabout theevolutionofthe firstfeathers is the difficultyin accounting for the genesis of the structurethrougha continuoussequence of selectiveforcesand witha continuous series
35 This content downloaded from 129.219.247.033 on October 07, 2016 14:34:33 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
36
THE QUARTERLY REVIEW OF BIOLOGY
of hypotheticalmorphological steps that are functionallyplausible. I shall attemptto formulate a model of feather evolution that gives particularattentionto the need forclear identificationof selectiveforces and to the need for functionalcontinuityattending any proposed morphologicaltransition.The model, of course, is speculative,since the available fossilfeather material is scanty and is difficultto place in phylogenetic sequence with any confidence. The model is not merelyan attemptto present a scheme that will withstandtestingand criticism. It is also an attempt to define as fully as possible the range of problems that must be dealt with in considering the origin of feathers. Any comprehensive scheme for the evolutionaryorigin of feathers must address itself simultaneouslyto several questions. Prominent among these is the problem of identifyingthe selective pressures that produced the first feathers.Were the firstfeatherseffectiveprimarilyin flightor gliding,or were theyeffective primarilyin heat transfersituations?Another importantquestion concernsthe detailed architectureof the feathers.How did the branching structureof shaft,barbs, and barbules evolve? How did the systemof tinyhooks and overlapping barbules that binds the feather surface into a pennaceous web evolve? The structure is so complex that it is simply not enough to suppose thatonce the scale had become frayed and perhaps down-like,hooked barbules were somehow added to the filamentousstructures to produce a flat,strong,flexible vane, as in the modern feather (an idea implicitin some literature).Indeed, the intermediatestructure that must be envisaged when one adds hooks to the filamentsof a down-likestructurecould resultin a tangledmess, more like a briar patch than a contour feather.Such failure clearly to outline intermediatesteps in the evolution of feathersand to justifythe hypotheticalstructures in terms of their adaptive value to the individual pervades the literatureon this subject. The model to be presentedhere willbe based in large part on a considerationof lizard scales. I do not wish to imply,however, that feathers derived fromlizard scales. Birds, of course, did not evolve from lizards. They did not even evolve fromlepidosaurian reptiles.The closest livingrelativesof birds are crocodilians,if one
[VOLUME
50
accepts that the derivation of crocodilians, dinosaurs, and birds is from the Thecodontia (Bock, 1969; Brodkorb, 1971). Among living reptiles, the crocodilians are similar to birds and unlike other reptiles,not only in certain aspects of their anatomy,but also in that,like birds, they build and guard nests, guard the young after hatching (Cott, 1971), and use sounds in communicationbetween motherand young as well as between males and females. Birds and crocodilians are also unusual and similar in that stones are taken up into a muscular portion of the stomach, where they possiblyaid in digestion.So the avian gizzard, while oftenconsidered an adaptation for flight (Welty,1962), may simplyreflectthe thecodont origin of birds. It is logical to assume thatwe should examine the integumentof crocodiles and alligators to gain insightintothe originsof the avian integument. Crocodilians,however,are highlymodified for aquatic life. The integument of a crocodilianmay not offerus any special insight into the conditionof the pre-avianintegument. On the other hand, many of the lizards, such as Sceloporusand Agama, have raised leaf-like scales on their bodies, neck regions, and tails and legs (Fig. 1). The effectis verymuch like a series of overlapping shingles on a roof. In the lizards mentioned, each shingle-likescale is raised, forming an opening between the underside of the anterior scale and the top surface of the posterior scale. Other lizards, for example, skinks,have large leaf-likeoverlapping scales thatare notraised butare pressed tightlyagainst one another, exactly like the shingleson a roof. It is from a consideration of the heat transferpropertiesof large, raised scales such as those on Sceloporusthat I believe we can make some progress in understanding the evolution of feathers.These scales will be shown to functionas a heat or radiation shield. Since thermoregulationis an important present-day functionof bird feathers,and since we can demonstrateinstanceswhere the evolution of enlarged scales on reptiles is probably a result of thermal selective pressures in the environment,the relationship between these twoobservationsshould be seriouslyconsidered forwhateverlightit mayshed on the evolutionary origin of feathers. The followingessay is divided intofivemajor sections. The firstsection deals criticallywith
This content downloaded from 129.219.247.033 on October 07, 2016 14:34:33 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c).
1975]
MARCH
ORICIN OF FEATHERS
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