You thought sparrows were boring? It turns out that these plucky little birds effectively have four sexes, where one sparrow can only mate with 1/4 of the population (instead of 1/2). White females only mate with tan males (not white males), and tan females only mate with white males (98.5% of pairings). This is due to the unusual action of a "supergene" on chromosome 2 that modifies color, behaviour, and mating preference.
What the heck?
Here's how it works. White-throated sparrows have two different color morphs, white and tan (kind of like how we could be blonde or brunette). And when they pair up, they almost always choose to pair up with an opposite color morph. So, white females exclusively prefer to pair up with tan males, while tan females always go for white males. This is called assortative mating, and a staggering 98.5% (1,099 out of 1,116) sparrows paired up with an opposite color birds (rather than white-white or tan-tan pairings).
Thus, this species actually has what we could call four different sexes-- the white females, tan females, white males, and tan males. Further, there are clear behavioral differences: white males are promiscuous, trying to mate with other females instead of taking care of offspring, while tan males are monogamous and invest in their brood-- and the same behaviors are seen in white and tan females, respectively.
You're probably wondering what explains this behavior, and if you're like me, you're murmuring to yourself "well, I guess opposites attract..."
But it turns out it is more complicated than that. Within the DNA on chromosome 2 of white-throated sparrows, there is a "supergene:" a cluster of related genes that are always inherited together (instead of recombining) because of a genetic "protective" mechanism. It is standard for genes that are physically closer together on a chromosome to be inherited together more often, but "supergenes" take advantage of an inherent protective "secret service" that prevents any recombination. What is protecting these genes from splitting up? A long inversion, or a section of the chromosome which is oriented backwards (EDCBA instead of ABCDE). When two chromosomes try to pair up, the inversion stops the chromosomes from pairing correctly and swapping genes back and forth.
Thus, the supergenes never split into component parts, and within this supergene, scientists have identified several genes with hypothesized function-- for example, one gene relates to coloration. and probably contributes to the white vs tan divide.
Several mysteries remain. First, it makes sense that white females would exclusively prefer to mate with tan males, who are monogamous and invest in their offspring. But why on earth would tan females exclusively want to mate with white males, who seek extra-pair matings and are not as interested in parental care?
Secondly, same-color-pairings were much more common in situations where the original pair lost one member (due, e.g., to death). In that case, 8/10 of the secondary pairings was with a same color individual (versus 9/1006 of the primary pairings). Why?
And finally, this system closely mimics the evolution of sex chromosomes. The two types of chromosome 2 (the white and tan versions) are analogous to X and Y chromosomes in an early stage of evolution. Are we witnessing a halfway stage in the evolution of new sex chromosomes in these sparrows?
Images from Tuttle et al. (2016) (left) and Cephas (creative commons, wiki)
Thanks to Professor David Haig for sending along relevant papers and discussing them!
This species comprises two morphs, tan and white, that differ in pigmentation and components of social behavior [ 3–5 ]. Morph is determined by alternative alleles at a balanced >100-Mb inversion-based supergene, providing a unique system for studying gene-behavior relationships. Using over two decades of field data, we document near-perfect disassortative mating among morphs, as well as the fitness consequences of rare assortative mating. ... We provide evidence that the “white” allele may be degrading, similar to neo-Y/W sex chromosomes. We further show that the “tan” allele has surprisingly low levels of genetic diversity yet does not show several canonical signatures of recurrent positive selection. We discuss these results in the context of the origin, molecular evolution, and possible fate of this remarkable polymorphism.