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Avian Supergenes PERSPECTIVES EVOLUTION important role in generating biological diver- Lekking ruffs. From left to right, a female, an sity in taxa ranging from plants to humans. independent male, and a satellite male ruff. A third The mimetic wing patterns of butterflies are type of male ruff closely resembles the female. Recent Avian a particularly well-documented example of research has shed light on the genetic underpinnings of how supergenes can underlie complex ad- the ruff’s complex reproductive strategies (1, 2). aptations (4). However, knowledge of the supergenes genetic architecture of supergenes remains attraction and attempt to “steal” copula- limited, and the molecular mechanisms by tions. Faeder males (<1%) mimic females Genetic data reveal how which they can generate complex pheno- in their plumage and smaller size and also two complex bird mating types are unclear. The recent studies of the steal copulations. ruff (1, 2) and the white-throated sparrow (3) As Küpper et al. (1) and Lamichhaney et systems evolved provide critical advances to our understand- al. (2) now show, these three reproductive ing of these aspects of supergenes. behaviors and associated phenotypes are de- By Scott Taylor 1,2 and Leonardo Campagna1,2 Reduced recombination within super- termined by a ~4.5 Mb inversion located on genes is central to their evolution, allowing an autosome (see the figure). Independent s the extravagant displays of birds of multiple genes to be inherited as a single males carry two copies of the ancestral, non- paradise remind us, many birds go to linked unit and setting the stage for their inverted chromosome: They do not possess great lengths to pass their genes on coevolution. Inversions, chromosomal re- either ruff supergene. Satellites and faeders to the next generation. Recent papers arrangements where large portions of the have different supergenes: They each carry explore the genetic basis of the repro- DNA molecule are flipped, suppress local one ancestral haplotype and one morph-spe- ductive strategies in two bird species: recombination (5). Perhaps not surprisingly, cific version of the supergene. Females carry- Athe ruff (Philomachus pugnax) (1, 2) and the inversions harbor supergene complexes (4) ing either version of the supergene can also white-throated sparrow (Zonotrichia albicol- in groups that now include the ruff and the be identified by size or from their behavioral lis) (3). In each species, striking variation white-throated sparrow (1–3). In each of response to testosterone implantation (1). in both plumage and behavior is controlled these bird species, individuals can exhibit The white-throated sparrow is a com- in concert via the inheritance of coadapted strikingly different plumage and behavior mon North American bird with two equally gene complexes (supergenes) in large chro- that we can now link to genomic variation. abundant color morphs: white-striped and mosomal inversions. The similar ways in The ruff is a lek-breeding wading bird in tan-striped. White males invest in secur- which these independently evolved super- wetlands of northern Eurasia (6). Male ruffs ing mates at the expense of parental care, genes influence morphology and behavior occur as one of three morphs, each with a whereas tan males are monogamous and elucidate how complex phenotypes evolve distinct breeding strategy and appearance help to look after their young (7). A similar and are maintained. (see the photo). Independent males (80 to trade-off is also seen in females. The two Supergenes are two or more linked genes 95% of the population) are dominant hold- morphs are controlled by the presence of that are inherited together. They can play an ers of display sites, with diverse patterns of an inversion that harbors a large, ~100 Mb ornamented dark plumage. Satellite males supergene, roughly 10% of the genome (3, 8, (5 to 20%) are also ornamented, but with 9), and Tuttle et al. (3) have disentangled its 1Fuller Evolutionary Biology Program, Cornell Lab of white plumage. They do not defend display evolutionary origin. White birds carry one Ornithology, Cornell University, Ithaca, NY, USA. 2Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, sites, but rather visit the leks of indepen- copy of the supergene and one noninverted NY, USA. E-mail: [email protected] dent males, where they assist with female form, whereas tan birds only carry the non- PICTURES/CORBIS © WINFRIED WISNIEWSKI/MINDEN PHOTO: 446 29 JANUARY 2016 • VOL 351 ISSUE 6272 sciencemag.org SCIENCE Published by AAAS INSIGHTS inverted form (see the figure). White birds of the precise mechanism remains unknown cases, loci involved in the response to sex either sex nearly always mate with tan birds (3). Why do the supergenes persist despite hormones and plumage pigmentation exist of the opposite sex. these fitness costs? The answer is that each in the supergene and likely act in concert Although the supergenes of white- mating system allows alternative reproduc- to produce the alternative mating strategies throated sparrows and ruffs are both an- tive strategies to coexist as balanced poly- and their associated behaviors and morphol- cient, they have different origins. The ruff morphisms. Satellite and faeder ruffs are ogies. In two closely related crow species, supergenes arose from rearrangements in hypothesized to have fitness advantages that another putative inversion-generated super- the ruff genome. The faeder supergene ap- maintain these morphs at low frequencies gene also contains genes involved in pigmen- pears to have arisen ~3.8 million years ago (1, 2). Polymorphism in sparrows persists via tation and hormonal regulation (11). This via an inversion of the ancestral chromo- their mating pattern (white nearly always mechanism is different from that seen in the some. The satellite supergene may be a mates with tan, producing both tan and rhinoceros beetle (Trypoxylus dichotomus), product of rare recombination between the white offspring) and similar fitness benefits where differential sensitivity to growth hor- ancestral ruff chromosome and the faeder to either mating strategy (3). mones based on a single signaling gene has supergene that took place ~0.5 million years Although the ruff and sparrow supergene been proposed as a molecular mechanism by ago (2). In contrast, in white-throated spar- variants can each be unambiguously linked which ornaments and weapons can grow to rows, Tuttle et al.’s phylogenomic analyses to morph-specific traits, moving past this exaggerated proportions (12). indicate that the supergene predates the ex- general association will be challenging. Each Considered in concert, the findings in ruff istence of that species and may be the prod- supergene region contains from 100 (ruff) to and white-throated sparrow highlight the uct of introgression via hybridization with a over 1000 (white-throated sparrow) genes, importance of supergenes in the generation now extinct relative (3). all of which are highly differentiated from of complex phenotypes. They provide insight In other taxa, supergenes and their poten- their respective noninverted haplotypes (1– into the varied ways in which supergenes can tially adaptive gene complexes have spread 3). The divergent alleles on the supergenes be generated and maintained and begin to ex- via hybridization (4), but the relative im- could drive differentiation between morphs, pose their genetic architecture. These recent portance of hybridization versus intraspe- yet there is evidence that the supergenes are studies provide a link between genotype and Ruf (Philomachus pugnax) White-throated sparrow (Zonotrichia albicollis) Independent Satellite Faeder Tan morph White morph Supergene Noninverted ( 1000 genes) Dull plumage Bright plumage Supergene Supergene Submissive High aggression Ancestral ( 100 genes) ( 100 genes) High parental care Low parental care Dark plumage Light plumage Female plumage Infrequent song displays Frequent song displays Territorial Not territorial Not territorial Disassortative mating Disassortative mating The genetic architecture of two avian mating systems. The presence of inversion-generated supergenes determines morphological and behavioral traits in ruffs and white- throated sparrows. The ruff supergenes harbor close to 100 genes; the white-throated sparrow supergene is much larger, with over 1000 genes. cific chromosomal rearrangements for the degrading (1–3), as is the case for the mam- phenotype, a long-standing goal in evolution- generation of supergenes is not known. The malian Y and avian W sex chromosomes (10). ary biology research. Supergenes may have recent studies (1–3) show that supergenes Typically, experimental crosses can be an underappreciated role in the generation with similarly complex influences on mor- used to tease apart regions of the genome of biodiversity, one that we are now poised phology and behavior can arise in both ways. involved in generating a trait. However, the to more fully appreciate and understand. ■ It remains to be shown whether supergenes lack of recombination within supergenes tend to be the product of within-species pro- makes this an unfeasible approach. Now REFERENCES 1. C. Küpper et al., Nat. Genet. 10.1038/ng.3443 (2016). cesses, or are more often co-opted from other that the genes within the ruff and white- 2. S. Lamichhaney et al., Nat. Genet. 10.1038/ng.3430 (2016). species via introgressive hybridization. throated sparrow supergenes are known and 3. E. M. Tuttle et al., Curr. Biol. 10.1126/j.cub.2015.11.069 In both birds, there are fitness conse- the genomic resources for these nonmodel (2016). quences associated with possessing the organisms have been generated, the rela- 4. T. Schwander et al., Curr. Biol. 24, R288 (2014). 5. L. H. Rieseberg, Trends Ecol. Evol. 16, 351 (2001). supergene, yet the polymorphisms appear tive influence of different genes in each su- 6. J. G. van Rhijn, The Ruff (Poyser, London, 1991). demographically stable. The ruff super- pergene can be explored with targeted gene 7. E. M. Tuttle, Behav. Ecol. 14, 425 (2003). SCIENCE genes are lethal when either sex has a copy expression analyses and genome-editing 8.
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