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Prospects & Overviews Did the fire ant supergene evolve selfishly or socially? Yu-Ching Huang and John Wang
The genetic basis for animal social organization is poorly understood. Fire ants provide one of the rare cases where variation in social organization has been demonstrated to be under genetic control, which amazingly, segregates as a single Mendelian locus. A recent genetic, genomic, and cytological analysis revealed that this locus actually consists of over 600 genes locked together in a supergene that possesses many characteristics of sex chromosomes. The fire ant social supergene also behaves selfishly, and an interesting evolutionary question is whether the genes incorporated first into the social supergene were those for social adaptation, selfish genetic drive, or something else. In depth, functional molecular genetic analysis in fire ants and comparative genomics in other closely related socially polymorphic species will be required to resolve this question.
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Keywords: fire ant; polygyny; social chromosome; social polymorphism; Solenopsis invicta; supergene
Introduction Animal societies are extremely diverse, some species forming temporary associations, and others, including ants and humans, forming stable, complex societies [1–3]. Although the ants are a monophyletic group of social insects, en route to their colonization of much of the Earth’s landmasses, they have evolved various and numerous morphological, ecologi-
cal, and life history adaptations, including different society organizations [2]. One of the most important organizing features of an ant colony is the number of queens [4, 5]. Monogynous colonies are headed by a single queen, and colony members typically are close relatives with aligned “genetic interests”. Polygynous ones are headed by multiple queens with less, or even little, genetic relatedness among colony members, sometimes creating genetic conflicts of interest. Despite the commonness of both monogynous and polygynous societies within an ant species or among closely related ant species, not much is known about the genetic bases for their regulation or variation. Most of what is known comes from extensive studies in the fire ant Solenopsis invicta, which is native to South America and a nasty invasive pest in many countries [6–10]. In this species, a single Mendelian locus explains intraspecific polymorphism in queen number [11–15]. Recently, this locus was shown to be a supergene composed of 600 genes locked together by a large inversion and possessing many characteristics of sex chromosomes [16]. This locus also behaves selfishly [17], and an interesting question is whether the genes incorporated first into the social supergene were those for social adaptation, selfish genetic drive, or something else (or possibly simultaneously). Understanding the fire ant system is of broad interest because it is a model for how evolutionary innovation could arise [18, 19]. We begin by introducing the fire ant social system; we discuss the supergene with regard to its gene-to-phenotype relationships and its evolutionary history; and we end with a brief proposition to study other ant systems with similar polymorphism in queen number.
Social polymorphism in fire ants DOI 10.1002/bies.201300103 Biodiversity Research Center, Academia Sinica, Taipei, Taiwan *Corresponding author: John Wang E-mail: [email protected] Abbreviations: CSP, chemosensory protein; CYP, cytochrome P450 enzyme; OBP, odorantbinding protein; OR, olfactory receptor.
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Fire ant social form polymorphism is associated with a single Mendelian element In the fire ant S. invicta, a single Mendelian element is perfectly associated with variability in social structure [15, 20, 21] (Fig. 1; for a detailed review see [12]). Colonies differ in queen number with some having one queen and others having multiple queens, sometimes hundreds [22, 23]. This fundamental difference in social organization is completely Bioessays 36: 200–208, ß 2013 WILEY Periodicals, Inc.
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associated with variation at the marker gene Gp-9, which has two alleles, B and b (Fig. 2A), and encodes a putative odorantbinding protein (OBP) [12, 14, 15, 17]. In the monogyne form, the queen and workers all have the Gp-9BB genotype. In contrast, polygyne colonies contain both Gp-9BB and Gp-9Bb workers, and interestingly, the queens of polygyne colonies are always Gp9Bb heterozygotes [15, 20]. The lack of the other two polygyne queen genotypes (Gp9BB and Gp-9bb) is due to two reasons. Behavioral studies have shown that workers marked by the Gp-9b allele selectively kill all queens without a copy (i.e. Gp-9BB queens); and Gp-9bb queens (and workers) are underrepresented and rarely reach adulthood [11, 17, 20, 24–26]. The acceptance of only queens having a Gp-9b allele by workers marked by a Gp-9b allele makes Gp-9b (a marker for) a behaviorally selfish gene, and in this case, a rare example of a “green beard” gene [17, 27]. Similar to other ants, monogyne and polygyne fire ant colonies also differ in many other aspects, with the phenotypes associated with the latter sometimes collectively called the “polygyne syndrome” [4, 5, 28]. New monogyne colonies are founded by single queens without workers whereas new polygyne colonies are founded by colony budding [28]. The former are territorial while the latter have less intercolony aggression [29]. At the individual level, both queens and workers are smaller, and queens are slower to mature, less fecund, and shorter-lived in polygyne colonies, as compared to monogyne ones. In fire ants, these phenotypes are also completely linked to Gp-9 genotype [25, 30]. Additionally and possibly specific to fire ants, Gp9Bb queens have more unsaturated hydrocarbons on the cuticle [31], and Gp-9b polygyne males have less sperm [32].
The Mendelian element is a supergene residing on a social chromosome Although one Mendelian element fully explains all these phenotypic differences between the monogyne and polygyne fire ant colonies, the presence of multiple tightly linked genes, possibly “locked” together in one or more inversions to form a supergene, has long been hypothesized [33, 34]. Recently, we and colleagues verified this suspicion through a series of
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Figure 1. Diagram of six phenotypic traits associated with social organization in fire ants. (1) Nest distribution. Monogyne nests often have an overdispersed distribution. Polygyne nests are often clustered and found at higher densities. (2) Intercolony aggression. Workers of different monogyne colonies behave aggressively toward each other (nuclear war symbol and gaster wagging [abdomens in up position]). Between polygyne colonies, workers exhibit less intercolony aggression, and individuals can move between colonies (peace sign). This difference in aggression helps explain the distribution of nests, above. (3) Queen number. Monogyne colonies are headed by a single queen, whereas polygyne colonies are headed by multiple queens. (4) Colony founding. Monogyne colonies are founded independently by a single newly mated queen after a nuptial flight. Newly mated polygyne queens typically join polygyne colonies instead of founding alone (return arrow). New polygyne colonies are founded by colony budding (smaller departing circle). (5) Queen size. The size of the head and thorax is the same between monogyne and polygyne queens. Monogyne queens have bigger and longer abdomens than polygyne queens because of greater fat accumulation and fecundity. (6) Worker size. The average worker mass is greater in monogyne colonies compared to polygyne ones. Other phenotypes discussed in text. Additional details in [12, 22].
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Figure 2. The social chromosomes in S. invicta. A: Social organization in S. invicta. In the invasive range, monogyne colonies contain a single queen with SB/SB genotype, whereas polygyne colonies contain multiple queens whose genotype are exclusively SB/ Sb. There is no acceptance of any queens from outside in monogyne colonies, regardless of the social chromosomes they possess. In polygyne colonies, however, only SB/Sb queens are accepted from outside: any SB/SB queens, which attempt to enter the colonies are inevitably executed. B: The monogyne queen (left) possesses homozygous social chromosomes (SB/SB), in which chromosomal crossovers can occur (dashed lines). The polygyne queen (right) possesses heterozygous social chromosomes (SB/Sb), in which recombination within the supergene is inhibited (denoted by lock symbols). C: Inversion model for social chromosome evolution. The ancestral SB chromosome evolves genes for either polygyny (a) or selfishness (b) first, and then a small-scale inversion occurs, suppressing local interallelic recombination (denoted by lock symbols) between the homologous chromosomes. Subsequently, genes for selfishness (a) or polygyny (b) are acquired and additional large-scale inversions further lock these genes together on the chromosome. Because of the inversion-induced recombination suppression, transposons and genetic differences can accumulate on the Sb supergene allele. The current Sb chromosome possesses both selfish and polygyne features. Other models are possible.
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genetic, genomic and cytological analyses [16]. Using restriction site associated DNA (RAD) sequencing [35], a method to genotype multiple individuals with next generation sequencing, we found that Gp-9 is part of a nonrecombining supergene composed of over 600 genes. The supergene spans approximately 13 megabases (55%) on a pair of “social chromosomes”, which are referred to as the “Social B” (SB) and “Social b” (Sb) chromosomes based on their respective Gp-9 alleles. The lack of recombination between the SB and Sb supergene alleles is due in part to a large 9 Mb inversion identified by bacterial artificial chromosome fluorescent in situ hybridization (Fig. 2B). In addition, the
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The social chromosomes resemble sex chromosomes and genetic drive complexes The social chromosomes share many of the properties of sex chromosomes [36, 37]. The Sb chromosome is only found in polygynous colonies and in a heterozygous state (SB/Sb) in reproductive queens, similar to the Y chromosome in males. Recombination is normal in SB/SB queens of the monogyne social form, as for XX females. However, Sb/Sb reproductive queens are inviable, hence recombination is not possible between Sb alleles. Lack of recombination allows the accumulation of deleterious mutations, including transposons and other repetitive sequences, such as those found on the Y chromosome. Additionally, many of the genes exhibiting expression differences between individuals of the two social forms are within the supergene on the social chromosomes [16, 38, 39]. These genes are presumably beneficial to their respective social forms, analogous to the X and Y chromosome having genes beneficial to females and males, respectively [40]. In addition to resembling sex chromosomes, the social chromosome has similarities to other chromosomes having selfish drive complexes, especially the t-locus in mice and Segregation Distorter in Drosophila melanogaster [41–44]. In both of these systems, heterozygous males transmit the selfish drive complex to nearly all of their offspring in a mechanism whereby the non-drive containing spermatids are inactivated. For these drive systems to work, multiple co-adapted loci must be genetically linked in regions of suppressed recombination, which are often facilitated by one or more inversions [41, 42]. The driving alleles do not fix in the population because they accumulate recessive lethals and other deleterious mutations, as has likewise occurred for the Sb allele. The recessive lethals and the deleterious mutations come with a fitness cost, and there may be selection for non-drive-allele-linked (i.e. SB in fire ants) or unlinked modifiers to reduce the transmission bias [45]. Such modifiers exist for both the t-locus and Segregation Distorter [42, 46, 47], although whether they are adaptive in natural populations or incidental byproducts of genetic variation is unclear [42]. Suppressors for transmission of the Sb chromosome can be in the form of accepting reproductive SB/SB queens. However, this does not appear to occur in fire ants in the invasive range where the polygyne phenotype appears fully linked to the Gp-9b allele (which is presumably also fully linked to the Sb supergene allele) [15, 20]. However, in invasive polygyne colonies a small percentage of virgin SB/SB queens do escape aggression and can take part in mating flights [11, 48, 49]. This has been hypothesized to be a form of developmental delay [12], and if there is a genetic component, can be viewed as a type of transmission suppression. In the native range, the genetic association between Gp-9 and social form is similar to the invasive range (although with much lower sample sizes [50]): monogyne colonies only have the Gp-9B-like alleles while Bioessays 36: 200–208, ß 2013 WILEY Periodicals, Inc.
polygyne colonies always have some Gp-9b-like alleles [14, 15, 20, 51, 52]. However, it remains to be determined if the two Gp-9 allele families are linked to respective SB-like and Sb-like supergenes. This may be likely given that the polygyne and (the inferred) selfish phenotypes are probably encoded by multiple genes. Accordingly, more or stronger suppressors of transmission for Sb-like supergenes (either in acceptance or surviving until mating flight) perhaps may occur in the native range where greater genetic variability is present [53, 54].
What are the gene-to-phenotype relationships in the supergene? Much remains to be learned about the fire ant supergene. One goal is to understand the mechanistic details of how the supergene works. For example, are the phenotypes associated with the supergene mostly the product of transcriptional or protein coding changes? In addition, what are the gene-tophenotype relationships associated with the polygyne syndrome or with the selfish acceptance of SB/Sb queens by workers in polygyne colonies?
Gene expression evolution may play a greater role than protein evolution The available data may tentatively suggest that gene expression plays a greater role than protein coding changes in generating the phenotypes associated with the supergene. From six sets of microarray or RNA-seq experiments, 53 genes within the supergene have been identified as differentially expressed, including 31 with SB or Sb allele-specific expression [16, 38, 39]. In contrast, only 21 genes could have functional protein coding changes based on potential evidence for positive (or relaxed) selection (n ¼ 16) or missing exons (n ¼ 5) [12, 14, 16, 52]. However, whether gene expression actually has the greater role will need to await additional data because some of the gene expression changes may have no phenotypic consequence. Also, the numbers of genes for both classes likely will increase with additional expression experiments and more extensive molecular evolution analyses.
Which genes mediate queen acceptance? In a step toward uncovering gene-to-phenotype relationships, a recent gene expression study compared SB/SB and SB/Sb queens at three different adult time points to determine which genes might be functionally important in their phenotypic differences [38]. One of the findings was that many genes associated with reproductive maturation rate were expressed in a manner consistent with the known faster maturation rate during early adulthood of SB/SB individuals, as compared to SB/Sb ones. Another result was that the expression of six fatty acid desaturase genes was higher in SB/Sb individuals, in comparison with SB/SB individuals. Although requiring verification by functional tests, such as RNA interference (e.g. [55, 56]), this likely explains the greater amount of
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accumulation of repetitive sequences on the Sb chromosome and at least one additional minor inversion between the SB and Sb chromosomes are likely to contribute to recombination suppression.
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unsaturated hydrocarbons found on the cuticle of SB/Sb queens, as compared to SB/SB queens, in both maturing and reproductive individuals [31]. Interestingly, three of the desaturase genes are not located in the supergene, and the remaining three have unknown chromosomal locations. This implies that their gene expression must be, directly or indirectly, controlled from within the supergene by a regulator (e.g. transcription factor), which remains to be identified. A speculative possibility for the indirect regulation of the desaturase genes may involve OBPs or the related chemosensory proteins (CSPs). While “canonical” sensory OBPs/ CSPs deliver odors to olfactory receptors (ORs), some putative OBPs/CSPs are not expressed in sensory organs, and they have been proposed to be carriers of lipids or other endocrine signals [57, 58]. In this model, “non-canonical” OBPs/CSPs would transport unsaturated hydrocarbons away from the site of synthesis to the cuticle more efficiently in SB/Sb queens, as compared to SB/SB ones. Possibly because of end product feedback inhibition (e.g. analogous to cholesterol metabolism [59]), the depletion of unsaturated hydrocarbons then would induce their own synthesis by the upregulation of the desaturases (and possibly other genes). Within the supergene there are 12 such candidate genes (seven OBPs and five CSPs). Of these, and as previously suggested, Gp-9 is an major candidate because it is expressed throughout the body and because the Gp-9B and b alleles encode amino acid differences predicted to be important for ligand binding [12, 14, 50, 52, 60]. Other interesting candidates are the three OBPs and one CSP that are differentially expressed between adult queens of alternate SB/SB and SB/Sb genotypes [38]. Polygyne workers accept or reject queens of alternate genotypes based on a cuticular label, which may be the aforementioned unsaturated hydrocarbons or some other cue [17, 31]. The discrimination could be at the level of chemosensory perception in the antennae where workers of alternate genotypes may express different alleles, gene combinations, or levels of the seven OBPs, five CSPs, and seven ORs found within the supergene. Of these, two OBPs and one CSP are differentially expressed between adult workers of alternate SB/SB and SB/Sb genotypes [39]. Alternatively, or in addition, allelic differences in or differential expression of key neural genes in the brain may result in distinct responses.
Which gene causes recessive lethality in Sb/Sb females? While the genes underlying queen odor and worker recognition contribute to the social form differences, the Sb allele of the supergene also carries one or more recessive lethal mutations that are incompletely penetrant in females [20, 24]. Two proposed causes for lethality include developmental defects [20, 24] and culling based on the frequency of other supergene genotypes in the social environment [26]. A previous study suggested that a single amino acid change encoded by the Gp-9b allele (lysine rather than glutamic acid at residue 151), but not by the Gp-9b-like alleles, was responsible for the lethal effect, although tightly linked genes could not be excluded [24]. Within the Sb supergene, six genes
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may be candidates for the tightly linked genes: five genes are likely loss-of-function mutations because they have one or more exon deletions and one gene has a transposon that interrupts its coding region. Of the five genes with deleted exons, two encode cytochrome P450 enzymes (CYPs), which are involved in the metabolism of both endogenous compounds and xenobiotics [61, 62]. The mutations in these two CYPs, if they function in the synthesis of hormones (e.g. juvenile hormone or ecdysone), could underlie the suspected developmental defects in Sb/Sb individuals. Alternatively, or in addition, the lethality may be caused by one or more of the genes with demonstrated (n ¼ 51) or yet to be identified altered gene expression levels, some of which may be caused by transposon insertions.
Which roles do transposons play? Both the queen and worker gene expression studies identified differentially expressed transposons, most of which were more highly expressed in SB/Sb individuals, likely because they are inserted into the Sb allele of the supergene [16, 39]. Some of the transposons may modulate gene expression or even have been domesticated, or exapted [63, 64]. Thus, an interesting question is to determine which transposon insertions are functionally relevant, especially for the polygyne associated phenotypes. That Sb is a sink for existing fire ant transposons raises the possibility that Sb could also be a bridgehead for the arrival of transposons new to fire ants, similar to the early colonization of Y chromosomes by transposons [40]. The horizontal transfer of transposons is likely to involve intermediate vectors such as viruses, parasites, or parasitoids, and intracellular symbiotic organisms [65]. Because the infection rates for viruses and microsporidia are higher in polygynous colonies relative to monogynous ones [66, 67], the horizontal transfer of transposons is more likely to occur in the former (which has Sb). Once inserted onto Sb, the new transposon might proliferate within the genome and spread within fire ants, at least in polygyne populations. The spread of the transposon may be rapid, as examples of new transposons sweeping to fixation or nearly so within 100 years have been documented in several Drosophila species [68–70]. In essence, the current genetic and genomic studies have only scratched the surface on how the supergene functions, and really only by suggesting candidate genes. We anticipate that future experiments will clarify the functional roles of the genes and genetic networks within the supergene, which may aid the development of novel fire ant control strategies and methods. Furthermore, knowing the gene-to-phenotype map will also help us understand the evolution of the fire ant social supergene, to which we turn next.
What was the evolutionary history of the heteromorphic social chromosomes? The evolutionary history of the heteromorphic social chromosomes is unknown. One interesting question is whether the divergence of SB and Sb predated speciation or whether Bioessays 36: 200–208, ß 2013 WILEY Periodicals, Inc.
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How old are the social chromosomes? The origin of the heteromorphic social chromosomes in fire ants was estimated to be 390,000 years ago [16]. This date appears too young to be prior to the speciation of the five known (and likely several additional cryptic) socially polymorphic fire ant species from their most recent common ancestor in S. America. Since hybridization can occur between Solenopsis species [72–75], the supergene could have introgressed across species [71]. Its subsequent, presumably, rapid spread to high frequencies may have been due to neutral drift but is likely to have been facilitated by its selfish nature, selection for polygyny, or selection for a linked trait. Thus, the social chromosomes could conceivably be young [12, 14, 71]. The age of recombination cessation may be underestimated based on several simplifying assumptions used for the original analysis. First, the molecular divergence rate between the two leafcutter ants used to calibrate divergence may be abnormally fast [76]. Second, large simple inversions typically only have reduced recombination near the breakpoints; genetic exchange can still occur in the interior by rare double recombination or gene conversion events [77, 78]. Third, multiple molecular strata, which are different chromosomal segments where recombination has ceased at different times often due to separate inversion events [37, 40], may be present between the two heteromorphic social chromosomes. As a result, age estimates would reflect a weighted average of all the strata.
Examining molecular strata may help reveal the evolutionary history of the fire ant social chromosomes Molecular strata may be present for the social chromosomes because, from a comparative standpoint, the evolution of the similar sex and selfish drive chromosomes often occur via the accumulation of multiple strata [37, 40]. Indeed, cloning of one of the inversion breakpoints has revealed a likely 1 Mb sub-inversion within the larger 9 Mb inversion (unpublished data). The strata model raises an interesting evolutionary question for the supergene. Which came first, the “polygyny syndrome” or the selfish gene (Fig. 2C)? If the genes encoding the selfish behavior are determined to reside on the oldest strata, then the simplest interpretation is that selfishness came first. Conversely, if the selfish genes are found on one of the younger strata, then some subset of the genes for the polygyne syndrome was probably recruited into the supergene first. There are some caveats to these simple conjectures. The first is that a gene on the earliest stratum may have evolved its current function much later, possibly after younger Bioessays 36: 200–208, ß 2013 WILEY Periodicals, Inc.
strata have been added into the supergene. Second, unlike the mammalian Y chromosomes where most of the genes have degenerated [79], there are a daunting number of genes to characterize (600) both by molecular evolution and phenotypic analyses. Some genes might play subtle but important roles in either selfishness or polygyny (or other) that may be overlooked if only strong phenotypes are taken into account. Third, maybe polygyny and selfishness were recruited into the supergene at the same time. Nevertheless, knowing the strata location of key genes will at least hint at a possible model for subsequent analyses. Experiments to conclusively determine the relative age and detailed architecture of the social supergene are clearly necessary to unravel its interesting history. Such experiments include genetic linkage analysis between the respective SBlike and Sb-like alleles of the native population of S. invicta as well as other closely related social polymorphic fire ant species. Likewise, extensive molecular evolution analyses need to be conducted for both gene sequences inside and outside of the supergene among the fire ant species, just as has been done for Gp-9 [14, 51, 52]. Cloning of the physical breakpoints will give detailed structural resolution of the SB-like and Sb-like alleles, but may be challenging because many inversions occur at repetitive sequences, which are often difficult to clone and assemble. Finally, gene manipulation (e.g. RNAi [55, 56]) and molecular biology experiments will be needed to ascertain which genes within the supergene are mere hitchhikers and which have a functional role, such as in selfish behavior or regulating social organization.
Do social supergenes for queen number exist in other ants? The existence of a fire ant social chromosome raises the question of whether social chromosomes or supergenes exist in other ants or social insects (see also [19] for other potential cases). We suggest examining the following four ant species, which have some support for a genetic basis for social polymorphism: Solenopsis geminata [52, 80], Formica selysi [81, 82], Messor pergandei [83, 84], and Leptothorax acervorum [85]. Studying S. geminata, a relatively distantly related fire ant in the “N. American” clade, would allow testing if a supergene was already present in the most recent common ancestor of the N. and S. American (which includes S. invicta) lineages. Alternatively, it may have independently evolved a social supergene, possibly with similar structure on the same homologous social chromosome. Several examples from vertebrate evolutionary genomic studies have revealed that repeated evolution can occur at chromosomal hotspots within and among species, some of which can have almost identical breakpoints [86–91]. Studying the latter three species would reveal whether the independent evolution of supergenes has occurred. Their existence would suggest that supergenes are not rare, and possibly frequent, for social polymorphisms. Furthermore, by comparing supergenes among species, it would be possible to determine if the same or similar types of genes are repeatedly recruited into the supergenes.
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introgression of Sb across species boundaries has occurred [12, 71]. Another goal is to determine the sequence of steps by which the supergene formed, which may (with additional molecular evolution analyses) inform us about the historical accumulation of phenotypes during fire ant supergene evolution [12].
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The lack of a supergene could also be illuminating. If multiple loci are identified, then polymorphic complex traits need not be genetically coupled. On the other hand, the presence of only one locus (i.e. a single gene) could imply that a master regulatory element or pathway is involved. This would be analogous to condition-dependent polyphenism in organismal development, which is often regulated by only one or a few key signaling pathways. Examples include dauer (a state of diapause) formation in Caenorhabditis elegans [92] and many insect polyphenisms (reviewed in [93]), such as queen versus worker caste determination [94–97] and nurse versus forager division of labor [98]. Genetic polymorphisms in analogous social regulatory genes may partially or fully alter complex social phenotypes. Consistent with this possibility, the gemini transcription factor has been implicated in the control of selfish worker reproduction in the Cape honeybee (Apis mellifera capensis) [99].
Conclusions Extensive genetic analysis in fire ants has revealed a supergene for social behavior. The fire ant social supergene still has many unknowns. Most notably is the question of its evolutionary history and origin: selfish or social first. Unraveling this will require additional detailed comparative evolutionary analysis among the closely related fire ant species as well as functional tests for the genetic mechanisms of important genes within the supergene. As sequencing technologies improve, genetic analysis of other species with social polymorphism in queen number will become more feasible. In the hopefully not too distant future, the question of whether supergenes for social behavior are common or rare will be answered.
Acknowledgments The authors would like to thank two anonymous reviewers for comments that improved the manuscript. This work was supported by the Biodiversity Research Center (Academia Sinica, Taiwan) and by Taiwan NSC grants #100-2311-B-001015-MY3 and # 101-2621-M-001-006. Y.-C. H is supported by a post-doctoral fellowship from Academia Sinica. The authors have declared no conflict of interest.
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Prospects & Overviews Did the fire ant supergene evolve selfishly or socially? Yu-Ching Huang and John Wang
The genetic basis for animal social organization is poorly understood. Fire ants provide one of the rare cases where variation in social organization has been demonstrated to be under genetic control, which amazingly, segregates as a single Mendelian locus. A recent genetic, genomic, and cytological analysis revealed that this locus actually consists of over 600 genes locked together in a supergene that possesses many characteristics of sex chromosomes. The fire ant social supergene also behaves selfishly, and an interesting evolutionary question is whether the genes incorporated first into the social supergene were those for social adaptation, selfish genetic drive, or something else. In depth, functional molecular genetic analysis in fire ants and comparative genomics in other closely related socially polymorphic species will be required to resolve this question.
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Keywords: fire ant; polygyny; social chromosome; social polymorphism; Solenopsis invicta; supergene
Introduction Animal societies are extremely diverse, some species forming temporary associations, and others, including ants and humans, forming stable, complex societies [1–3]. Although the ants are a monophyletic group of social insects, en route to their colonization of much of the Earth’s landmasses, they have evolved various and numerous morphological, ecologi-
cal, and life history adaptations, including different society organizations [2]. One of the most important organizing features of an ant colony is the number of queens [4, 5]. Monogynous colonies are headed by a single queen, and colony members typically are close relatives with aligned “genetic interests”. Polygynous ones are headed by multiple queens with less, or even little, genetic relatedness among colony members, sometimes creating genetic conflicts of interest. Despite the commonness of both monogynous and polygynous societies within an ant species or among closely related ant species, not much is known about the genetic bases for their regulation or variation. Most of what is known comes from extensive studies in the fire ant Solenopsis invicta, which is native to South America and a nasty invasive pest in many countries [6–10]. In this species, a single Mendelian locus explains intraspecific polymorphism in queen number [11–15]. Recently, this locus was shown to be a supergene composed of 600 genes locked together by a large inversion and possessing many characteristics of sex chromosomes [16]. This locus also behaves selfishly [17], and an interesting question is whether the genes incorporated first into the social supergene were those for social adaptation, selfish genetic drive, or something else (or possibly simultaneously). Understanding the fire ant system is of broad interest because it is a model for how evolutionary innovation could arise [18, 19]. We begin by introducing the fire ant social system; we discuss the supergene with regard to its gene-to-phenotype relationships and its evolutionary history; and we end with a brief proposition to study other ant systems with similar polymorphism in queen number.
Social polymorphism in fire ants DOI 10.1002/bies.201300103 Biodiversity Research Center, Academia Sinica, Taipei, Taiwan *Corresponding author: John Wang E-mail: [email protected] Abbreviations: CSP, chemosensory protein; CYP, cytochrome P450 enzyme; OBP, odorantbinding protein; OR, olfactory receptor.
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Fire ant social form polymorphism is associated with a single Mendelian element In the fire ant S. invicta, a single Mendelian element is perfectly associated with variability in social structure [15, 20, 21] (Fig. 1; for a detailed review see [12]). Colonies differ in queen number with some having one queen and others having multiple queens, sometimes hundreds [22, 23]. This fundamental difference in social organization is completely Bioessays 36: 200–208, ß 2013 WILEY Periodicals, Inc.
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associated with variation at the marker gene Gp-9, which has two alleles, B and b (Fig. 2A), and encodes a putative odorantbinding protein (OBP) [12, 14, 15, 17]. In the monogyne form, the queen and workers all have the Gp-9BB genotype. In contrast, polygyne colonies contain both Gp-9BB and Gp-9Bb workers, and interestingly, the queens of polygyne colonies are always Gp9Bb heterozygotes [15, 20]. The lack of the other two polygyne queen genotypes (Gp9BB and Gp-9bb) is due to two reasons. Behavioral studies have shown that workers marked by the Gp-9b allele selectively kill all queens without a copy (i.e. Gp-9BB queens); and Gp-9bb queens (and workers) are underrepresented and rarely reach adulthood [11, 17, 20, 24–26]. The acceptance of only queens having a Gp-9b allele by workers marked by a Gp-9b allele makes Gp-9b (a marker for) a behaviorally selfish gene, and in this case, a rare example of a “green beard” gene [17, 27]. Similar to other ants, monogyne and polygyne fire ant colonies also differ in many other aspects, with the phenotypes associated with the latter sometimes collectively called the “polygyne syndrome” [4, 5, 28]. New monogyne colonies are founded by single queens without workers whereas new polygyne colonies are founded by colony budding [28]. The former are territorial while the latter have less intercolony aggression [29]. At the individual level, both queens and workers are smaller, and queens are slower to mature, less fecund, and shorter-lived in polygyne colonies, as compared to monogyne ones. In fire ants, these phenotypes are also completely linked to Gp-9 genotype [25, 30]. Additionally and possibly specific to fire ants, Gp9Bb queens have more unsaturated hydrocarbons on the cuticle [31], and Gp-9b polygyne males have less sperm [32].
The Mendelian element is a supergene residing on a social chromosome Although one Mendelian element fully explains all these phenotypic differences between the monogyne and polygyne fire ant colonies, the presence of multiple tightly linked genes, possibly “locked” together in one or more inversions to form a supergene, has long been hypothesized [33, 34]. Recently, we and colleagues verified this suspicion through a series of
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Figure 1. Diagram of six phenotypic traits associated with social organization in fire ants. (1) Nest distribution. Monogyne nests often have an overdispersed distribution. Polygyne nests are often clustered and found at higher densities. (2) Intercolony aggression. Workers of different monogyne colonies behave aggressively toward each other (nuclear war symbol and gaster wagging [abdomens in up position]). Between polygyne colonies, workers exhibit less intercolony aggression, and individuals can move between colonies (peace sign). This difference in aggression helps explain the distribution of nests, above. (3) Queen number. Monogyne colonies are headed by a single queen, whereas polygyne colonies are headed by multiple queens. (4) Colony founding. Monogyne colonies are founded independently by a single newly mated queen after a nuptial flight. Newly mated polygyne queens typically join polygyne colonies instead of founding alone (return arrow). New polygyne colonies are founded by colony budding (smaller departing circle). (5) Queen size. The size of the head and thorax is the same between monogyne and polygyne queens. Monogyne queens have bigger and longer abdomens than polygyne queens because of greater fat accumulation and fecundity. (6) Worker size. The average worker mass is greater in monogyne colonies compared to polygyne ones. Other phenotypes discussed in text. Additional details in [12, 22].
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Figure 2. The social chromosomes in S. invicta. A: Social organization in S. invicta. In the invasive range, monogyne colonies contain a single queen with SB/SB genotype, whereas polygyne colonies contain multiple queens whose genotype are exclusively SB/ Sb. There is no acceptance of any queens from outside in monogyne colonies, regardless of the social chromosomes they possess. In polygyne colonies, however, only SB/Sb queens are accepted from outside: any SB/SB queens, which attempt to enter the colonies are inevitably executed. B: The monogyne queen (left) possesses homozygous social chromosomes (SB/SB), in which chromosomal crossovers can occur (dashed lines). The polygyne queen (right) possesses heterozygous social chromosomes (SB/Sb), in which recombination within the supergene is inhibited (denoted by lock symbols). C: Inversion model for social chromosome evolution. The ancestral SB chromosome evolves genes for either polygyny (a) or selfishness (b) first, and then a small-scale inversion occurs, suppressing local interallelic recombination (denoted by lock symbols) between the homologous chromosomes. Subsequently, genes for selfishness (a) or polygyny (b) are acquired and additional large-scale inversions further lock these genes together on the chromosome. Because of the inversion-induced recombination suppression, transposons and genetic differences can accumulate on the Sb supergene allele. The current Sb chromosome possesses both selfish and polygyne features. Other models are possible.
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genetic, genomic and cytological analyses [16]. Using restriction site associated DNA (RAD) sequencing [35], a method to genotype multiple individuals with next generation sequencing, we found that Gp-9 is part of a nonrecombining supergene composed of over 600 genes. The supergene spans approximately 13 megabases (55%) on a pair of “social chromosomes”, which are referred to as the “Social B” (SB) and “Social b” (Sb) chromosomes based on their respective Gp-9 alleles. The lack of recombination between the SB and Sb supergene alleles is due in part to a large 9 Mb inversion identified by bacterial artificial chromosome fluorescent in situ hybridization (Fig. 2B). In addition, the
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The social chromosomes resemble sex chromosomes and genetic drive complexes The social chromosomes share many of the properties of sex chromosomes [36, 37]. The Sb chromosome is only found in polygynous colonies and in a heterozygous state (SB/Sb) in reproductive queens, similar to the Y chromosome in males. Recombination is normal in SB/SB queens of the monogyne social form, as for XX females. However, Sb/Sb reproductive queens are inviable, hence recombination is not possible between Sb alleles. Lack of recombination allows the accumulation of deleterious mutations, including transposons and other repetitive sequences, such as those found on the Y chromosome. Additionally, many of the genes exhibiting expression differences between individuals of the two social forms are within the supergene on the social chromosomes [16, 38, 39]. These genes are presumably beneficial to their respective social forms, analogous to the X and Y chromosome having genes beneficial to females and males, respectively [40]. In addition to resembling sex chromosomes, the social chromosome has similarities to other chromosomes having selfish drive complexes, especially the t-locus in mice and Segregation Distorter in Drosophila melanogaster [41–44]. In both of these systems, heterozygous males transmit the selfish drive complex to nearly all of their offspring in a mechanism whereby the non-drive containing spermatids are inactivated. For these drive systems to work, multiple co-adapted loci must be genetically linked in regions of suppressed recombination, which are often facilitated by one or more inversions [41, 42]. The driving alleles do not fix in the population because they accumulate recessive lethals and other deleterious mutations, as has likewise occurred for the Sb allele. The recessive lethals and the deleterious mutations come with a fitness cost, and there may be selection for non-drive-allele-linked (i.e. SB in fire ants) or unlinked modifiers to reduce the transmission bias [45]. Such modifiers exist for both the t-locus and Segregation Distorter [42, 46, 47], although whether they are adaptive in natural populations or incidental byproducts of genetic variation is unclear [42]. Suppressors for transmission of the Sb chromosome can be in the form of accepting reproductive SB/SB queens. However, this does not appear to occur in fire ants in the invasive range where the polygyne phenotype appears fully linked to the Gp-9b allele (which is presumably also fully linked to the Sb supergene allele) [15, 20]. However, in invasive polygyne colonies a small percentage of virgin SB/SB queens do escape aggression and can take part in mating flights [11, 48, 49]. This has been hypothesized to be a form of developmental delay [12], and if there is a genetic component, can be viewed as a type of transmission suppression. In the native range, the genetic association between Gp-9 and social form is similar to the invasive range (although with much lower sample sizes [50]): monogyne colonies only have the Gp-9B-like alleles while Bioessays 36: 200–208, ß 2013 WILEY Periodicals, Inc.
polygyne colonies always have some Gp-9b-like alleles [14, 15, 20, 51, 52]. However, it remains to be determined if the two Gp-9 allele families are linked to respective SB-like and Sb-like supergenes. This may be likely given that the polygyne and (the inferred) selfish phenotypes are probably encoded by multiple genes. Accordingly, more or stronger suppressors of transmission for Sb-like supergenes (either in acceptance or surviving until mating flight) perhaps may occur in the native range where greater genetic variability is present [53, 54].
What are the gene-to-phenotype relationships in the supergene? Much remains to be learned about the fire ant supergene. One goal is to understand the mechanistic details of how the supergene works. For example, are the phenotypes associated with the supergene mostly the product of transcriptional or protein coding changes? In addition, what are the gene-tophenotype relationships associated with the polygyne syndrome or with the selfish acceptance of SB/Sb queens by workers in polygyne colonies?
Gene expression evolution may play a greater role than protein evolution The available data may tentatively suggest that gene expression plays a greater role than protein coding changes in generating the phenotypes associated with the supergene. From six sets of microarray or RNA-seq experiments, 53 genes within the supergene have been identified as differentially expressed, including 31 with SB or Sb allele-specific expression [16, 38, 39]. In contrast, only 21 genes could have functional protein coding changes based on potential evidence for positive (or relaxed) selection (n ¼ 16) or missing exons (n ¼ 5) [12, 14, 16, 52]. However, whether gene expression actually has the greater role will need to await additional data because some of the gene expression changes may have no phenotypic consequence. Also, the numbers of genes for both classes likely will increase with additional expression experiments and more extensive molecular evolution analyses.
Which genes mediate queen acceptance? In a step toward uncovering gene-to-phenotype relationships, a recent gene expression study compared SB/SB and SB/Sb queens at three different adult time points to determine which genes might be functionally important in their phenotypic differences [38]. One of the findings was that many genes associated with reproductive maturation rate were expressed in a manner consistent with the known faster maturation rate during early adulthood of SB/SB individuals, as compared to SB/Sb ones. Another result was that the expression of six fatty acid desaturase genes was higher in SB/Sb individuals, in comparison with SB/SB individuals. Although requiring verification by functional tests, such as RNA interference (e.g. [55, 56]), this likely explains the greater amount of
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accumulation of repetitive sequences on the Sb chromosome and at least one additional minor inversion between the SB and Sb chromosomes are likely to contribute to recombination suppression.
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unsaturated hydrocarbons found on the cuticle of SB/Sb queens, as compared to SB/SB queens, in both maturing and reproductive individuals [31]. Interestingly, three of the desaturase genes are not located in the supergene, and the remaining three have unknown chromosomal locations. This implies that their gene expression must be, directly or indirectly, controlled from within the supergene by a regulator (e.g. transcription factor), which remains to be identified. A speculative possibility for the indirect regulation of the desaturase genes may involve OBPs or the related chemosensory proteins (CSPs). While “canonical” sensory OBPs/ CSPs deliver odors to olfactory receptors (ORs), some putative OBPs/CSPs are not expressed in sensory organs, and they have been proposed to be carriers of lipids or other endocrine signals [57, 58]. In this model, “non-canonical” OBPs/CSPs would transport unsaturated hydrocarbons away from the site of synthesis to the cuticle more efficiently in SB/Sb queens, as compared to SB/SB ones. Possibly because of end product feedback inhibition (e.g. analogous to cholesterol metabolism [59]), the depletion of unsaturated hydrocarbons then would induce their own synthesis by the upregulation of the desaturases (and possibly other genes). Within the supergene there are 12 such candidate genes (seven OBPs and five CSPs). Of these, and as previously suggested, Gp-9 is an major candidate because it is expressed throughout the body and because the Gp-9B and b alleles encode amino acid differences predicted to be important for ligand binding [12, 14, 50, 52, 60]. Other interesting candidates are the three OBPs and one CSP that are differentially expressed between adult queens of alternate SB/SB and SB/Sb genotypes [38]. Polygyne workers accept or reject queens of alternate genotypes based on a cuticular label, which may be the aforementioned unsaturated hydrocarbons or some other cue [17, 31]. The discrimination could be at the level of chemosensory perception in the antennae where workers of alternate genotypes may express different alleles, gene combinations, or levels of the seven OBPs, five CSPs, and seven ORs found within the supergene. Of these, two OBPs and one CSP are differentially expressed between adult workers of alternate SB/SB and SB/Sb genotypes [39]. Alternatively, or in addition, allelic differences in or differential expression of key neural genes in the brain may result in distinct responses.
Which gene causes recessive lethality in Sb/Sb females? While the genes underlying queen odor and worker recognition contribute to the social form differences, the Sb allele of the supergene also carries one or more recessive lethal mutations that are incompletely penetrant in females [20, 24]. Two proposed causes for lethality include developmental defects [20, 24] and culling based on the frequency of other supergene genotypes in the social environment [26]. A previous study suggested that a single amino acid change encoded by the Gp-9b allele (lysine rather than glutamic acid at residue 151), but not by the Gp-9b-like alleles, was responsible for the lethal effect, although tightly linked genes could not be excluded [24]. Within the Sb supergene, six genes
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may be candidates for the tightly linked genes: five genes are likely loss-of-function mutations because they have one or more exon deletions and one gene has a transposon that interrupts its coding region. Of the five genes with deleted exons, two encode cytochrome P450 enzymes (CYPs), which are involved in the metabolism of both endogenous compounds and xenobiotics [61, 62]. The mutations in these two CYPs, if they function in the synthesis of hormones (e.g. juvenile hormone or ecdysone), could underlie the suspected developmental defects in Sb/Sb individuals. Alternatively, or in addition, the lethality may be caused by one or more of the genes with demonstrated (n ¼ 51) or yet to be identified altered gene expression levels, some of which may be caused by transposon insertions.
Which roles do transposons play? Both the queen and worker gene expression studies identified differentially expressed transposons, most of which were more highly expressed in SB/Sb individuals, likely because they are inserted into the Sb allele of the supergene [16, 39]. Some of the transposons may modulate gene expression or even have been domesticated, or exapted [63, 64]. Thus, an interesting question is to determine which transposon insertions are functionally relevant, especially for the polygyne associated phenotypes. That Sb is a sink for existing fire ant transposons raises the possibility that Sb could also be a bridgehead for the arrival of transposons new to fire ants, similar to the early colonization of Y chromosomes by transposons [40]. The horizontal transfer of transposons is likely to involve intermediate vectors such as viruses, parasites, or parasitoids, and intracellular symbiotic organisms [65]. Because the infection rates for viruses and microsporidia are higher in polygynous colonies relative to monogynous ones [66, 67], the horizontal transfer of transposons is more likely to occur in the former (which has Sb). Once inserted onto Sb, the new transposon might proliferate within the genome and spread within fire ants, at least in polygyne populations. The spread of the transposon may be rapid, as examples of new transposons sweeping to fixation or nearly so within 100 years have been documented in several Drosophila species [68–70]. In essence, the current genetic and genomic studies have only scratched the surface on how the supergene functions, and really only by suggesting candidate genes. We anticipate that future experiments will clarify the functional roles of the genes and genetic networks within the supergene, which may aid the development of novel fire ant control strategies and methods. Furthermore, knowing the gene-to-phenotype map will also help us understand the evolution of the fire ant social supergene, to which we turn next.
What was the evolutionary history of the heteromorphic social chromosomes? The evolutionary history of the heteromorphic social chromosomes is unknown. One interesting question is whether the divergence of SB and Sb predated speciation or whether Bioessays 36: 200–208, ß 2013 WILEY Periodicals, Inc.
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How old are the social chromosomes? The origin of the heteromorphic social chromosomes in fire ants was estimated to be 390,000 years ago [16]. This date appears too young to be prior to the speciation of the five known (and likely several additional cryptic) socially polymorphic fire ant species from their most recent common ancestor in S. America. Since hybridization can occur between Solenopsis species [72–75], the supergene could have introgressed across species [71]. Its subsequent, presumably, rapid spread to high frequencies may have been due to neutral drift but is likely to have been facilitated by its selfish nature, selection for polygyny, or selection for a linked trait. Thus, the social chromosomes could conceivably be young [12, 14, 71]. The age of recombination cessation may be underestimated based on several simplifying assumptions used for the original analysis. First, the molecular divergence rate between the two leafcutter ants used to calibrate divergence may be abnormally fast [76]. Second, large simple inversions typically only have reduced recombination near the breakpoints; genetic exchange can still occur in the interior by rare double recombination or gene conversion events [77, 78]. Third, multiple molecular strata, which are different chromosomal segments where recombination has ceased at different times often due to separate inversion events [37, 40], may be present between the two heteromorphic social chromosomes. As a result, age estimates would reflect a weighted average of all the strata.
Examining molecular strata may help reveal the evolutionary history of the fire ant social chromosomes Molecular strata may be present for the social chromosomes because, from a comparative standpoint, the evolution of the similar sex and selfish drive chromosomes often occur via the accumulation of multiple strata [37, 40]. Indeed, cloning of one of the inversion breakpoints has revealed a likely 1 Mb sub-inversion within the larger 9 Mb inversion (unpublished data). The strata model raises an interesting evolutionary question for the supergene. Which came first, the “polygyny syndrome” or the selfish gene (Fig. 2C)? If the genes encoding the selfish behavior are determined to reside on the oldest strata, then the simplest interpretation is that selfishness came first. Conversely, if the selfish genes are found on one of the younger strata, then some subset of the genes for the polygyne syndrome was probably recruited into the supergene first. There are some caveats to these simple conjectures. The first is that a gene on the earliest stratum may have evolved its current function much later, possibly after younger Bioessays 36: 200–208, ß 2013 WILEY Periodicals, Inc.
strata have been added into the supergene. Second, unlike the mammalian Y chromosomes where most of the genes have degenerated [79], there are a daunting number of genes to characterize (600) both by molecular evolution and phenotypic analyses. Some genes might play subtle but important roles in either selfishness or polygyny (or other) that may be overlooked if only strong phenotypes are taken into account. Third, maybe polygyny and selfishness were recruited into the supergene at the same time. Nevertheless, knowing the strata location of key genes will at least hint at a possible model for subsequent analyses. Experiments to conclusively determine the relative age and detailed architecture of the social supergene are clearly necessary to unravel its interesting history. Such experiments include genetic linkage analysis between the respective SBlike and Sb-like alleles of the native population of S. invicta as well as other closely related social polymorphic fire ant species. Likewise, extensive molecular evolution analyses need to be conducted for both gene sequences inside and outside of the supergene among the fire ant species, just as has been done for Gp-9 [14, 51, 52]. Cloning of the physical breakpoints will give detailed structural resolution of the SB-like and Sb-like alleles, but may be challenging because many inversions occur at repetitive sequences, which are often difficult to clone and assemble. Finally, gene manipulation (e.g. RNAi [55, 56]) and molecular biology experiments will be needed to ascertain which genes within the supergene are mere hitchhikers and which have a functional role, such as in selfish behavior or regulating social organization.
Do social supergenes for queen number exist in other ants? The existence of a fire ant social chromosome raises the question of whether social chromosomes or supergenes exist in other ants or social insects (see also [19] for other potential cases). We suggest examining the following four ant species, which have some support for a genetic basis for social polymorphism: Solenopsis geminata [52, 80], Formica selysi [81, 82], Messor pergandei [83, 84], and Leptothorax acervorum [85]. Studying S. geminata, a relatively distantly related fire ant in the “N. American” clade, would allow testing if a supergene was already present in the most recent common ancestor of the N. and S. American (which includes S. invicta) lineages. Alternatively, it may have independently evolved a social supergene, possibly with similar structure on the same homologous social chromosome. Several examples from vertebrate evolutionary genomic studies have revealed that repeated evolution can occur at chromosomal hotspots within and among species, some of which can have almost identical breakpoints [86–91]. Studying the latter three species would reveal whether the independent evolution of supergenes has occurred. Their existence would suggest that supergenes are not rare, and possibly frequent, for social polymorphisms. Furthermore, by comparing supergenes among species, it would be possible to determine if the same or similar types of genes are repeatedly recruited into the supergenes.
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introgression of Sb across species boundaries has occurred [12, 71]. Another goal is to determine the sequence of steps by which the supergene formed, which may (with additional molecular evolution analyses) inform us about the historical accumulation of phenotypes during fire ant supergene evolution [12].
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The lack of a supergene could also be illuminating. If multiple loci are identified, then polymorphic complex traits need not be genetically coupled. On the other hand, the presence of only one locus (i.e. a single gene) could imply that a master regulatory element or pathway is involved. This would be analogous to condition-dependent polyphenism in organismal development, which is often regulated by only one or a few key signaling pathways. Examples include dauer (a state of diapause) formation in Caenorhabditis elegans [92] and many insect polyphenisms (reviewed in [93]), such as queen versus worker caste determination [94–97] and nurse versus forager division of labor [98]. Genetic polymorphisms in analogous social regulatory genes may partially or fully alter complex social phenotypes. Consistent with this possibility, the gemini transcription factor has been implicated in the control of selfish worker reproduction in the Cape honeybee (Apis mellifera capensis) [99].
Conclusions Extensive genetic analysis in fire ants has revealed a supergene for social behavior. The fire ant social supergene still has many unknowns. Most notably is the question of its evolutionary history and origin: selfish or social first. Unraveling this will require additional detailed comparative evolutionary analysis among the closely related fire ant species as well as functional tests for the genetic mechanisms of important genes within the supergene. As sequencing technologies improve, genetic analysis of other species with social polymorphism in queen number will become more feasible. In the hopefully not too distant future, the question of whether supergenes for social behavior are common or rare will be answered.
Acknowledgments The authors would like to thank two anonymous reviewers for comments that improved the manuscript. This work was supported by the Biodiversity Research Center (Academia Sinica, Taiwan) and by Taiwan NSC grants #100-2311-B-001015-MY3 and # 101-2621-M-001-006. Y.-C. H is supported by a post-doctoral fellowship from Academia Sinica. The authors have declared no conflict of interest.
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