Supergenes and Sparrows with Four Sexes

Supergenes are groups of tightly-linked genes that influence suites of traits relevant to fitness. While long a fixture of evolutionary genetics theory, their role in empirical studies of non-model organisms has been relatively limited, due to limitations in both our understanding of genomic architecture and the fitness consequences of traits.

In a recent Current Biology paper on the evolutionary history and implications of a chromosmal inversion-based “supergene” responsible for white and tan color morphs of White-throated Sparrows (Zonotrichia albicollis), Elaine M. Tuttle and her coauthors overcome this hurdle with what one tweeted was “25 years of fieldwork and a pile of genomics.”

Alternate color morphs in male and female sparrows differ at alternate supergene alleles on chromosome 2, which is highly divergent and potentially the result of hybridization followed by adaptive introgression. Figure 1 from Tuttle et al. 2016.

Alternate color morphs in male and female sparrows differ at alternate supergene alleles on chromosome 2, which is highly divergent and potentially the result of hybridization followed by adaptive introgression. Figure 1 from Tuttle et al.

Those 25 years of field work prompted an investigation of the genomic architecture of a fitness-linked supergene by first documenting perfect “dissociative” mating between tan and white color morphs of sparrow. In other words, any individual bird is restricted to mating only with another bird of both the opposite sex chromosome and color morph supergene (approximately 1/4th of the total population).

Different color morphs of the same sex also displayed remarkably different social behavior: white morph males were highly promiscuous, but tan morph males were monogamous and contributed more to caring for offspring, while a similar pattern was seen in females. Very rare assortative mating events also apparently had severe fitness consequences, as some hybrid individuals were much smaller, potentially as a result of less parental investment.

De-novo whole genome sequencing and population genomics revealed that this dissociative mating results in 99.7% of white morph sparrows being heterozygous for alternative supergene alleles on the second chromosome, while tan morph sparrows are always homozygous.

How did these alternate copies come to exist? A phylogenomic analysis demonstrated the inversion-based supergene originated prior to the divergence of the White-throated Sparrow from its sister species, Harris’s Sparrow (Z. querula). Tuttle et al. posit that its polymorphism is best explained by hybridization with an unknown sister species followed by adaptive introgression of one chromosomal copy. Interestingly, as a result of complete homozygosity and an absence of recombination, this copy may now be degrading, similar to patterns seen in some sex chromosome systems.

The upshot of all this: White-throated Sparrows have effectively four sexes, from their chromosomes to their reproductive behavior. It’s a striking finding that testifies to the power of using long-term field data to put genomics in the context of organismal biology.

References:

Thompson, M.J., Jiggins, C.D. 2014. Supergenes and their role in evolution. Heredity 114. DOI: 10.1038/hdy.2014.20

Tuttle, E.M., et al. 2016. Divergence and Functional Degradation of a Sex Chromosome-like Supergene. Current Biology 26. DOI: 10.1016/j.cub.2015.11.069

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About Ethan Linck

I’m a Ph.D. Candidate at the Department of Biology and the Burke Museum of Natural History, University of Washington, Seattle. My research uses museum specimens and genomic data to analyze and archive avian biodiversity and evolution, particularly in western North America and Melanesia.

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