SUMMARY A major challenge in biology is to understand the genetic basis of adaptation. One compelling idea is that groups of tightly linked genes (i.e. ‘supergenes’ [1, 2]) facilitate adaptation in suites of traits that determine fitness. Despite their likely importance, little is known about how alternate supergene alleles arise and become differentiated, nor their ultimate fate within species. Herein we address these questions by investigating the evolutionary history of a supergene in white-throated sparrows, Zonotrichia albicollis. 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 >100Mb 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 use de novo whole genome sequencing coupled with population- and phylo-genomic data, to show that alternate supergene alleles are highly divergent at over 1,000 genes, that these alleles originated prior to the split of Z. albicollis from its sister species, and may be polymorphic in Z. albicollis due to a past hybridization event. We provide evidence that the ‘white' allele may be degrading, similar to neo-Y/Wsex 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.

How reproductive strategies contribute to patterns of senescence in natural populations remains contentious. We studied reproductive senescence in the dimorphic white-throated sparrow, an excellent species for exploring this issue. Within both sexes the morphs use distinct reproductive strategies, and disassortative pairing by morph results in pair types with distinct parental systems. White morph birds are more colorful and aggressive than tan counterparts, and white males compete for extrapair matings, whereas tan males are more parental. Tan males and white females share parental care equally, whereas white males provide little parental support to tan females. We found morph-specific patterns of reproductive senescence in both sexes. White males exhibited greater reproductive senescence than tan males. This result likely reflects the difficulty of sustaining a highly competitive reproductive strategy as aging progresses rather than high physiological costs of competitiveness, since white males were also long-lived. Moreover, morph was not consistently related to reproductive senescence across the sexes, arguing against especially high costs of the traits associated with white morph identity. Rather, tan females exhibited earlier reproductive senescence than white females and were short-lived, perhaps reflecting the challenges of unsupported motherhood. Results underscore the importance of social dynamics in determining patterns of reproductive senescence.

It is often hypothesized that intra-sexual competition accelerates actuarial senescence, or the increase in mortality rates with age. However, an alternative hypothesis is that parental investment is more important to determining senescence rates. We used a unique model system, the white-throated sparrow (Zonotrichia albicollis), to study variation in actuarial senescence. In this species, genetically determined morphs display discrete mating strategies and disassortative pairing, providing an excellent opportunity to test the predictions of the above hypotheses. Compared to tan-striped males, white-striped males are more polygynous and aggressive, and less parental. Tan-striped females receive less parental support, and invest more into parental care than white-striped females, which are also more aggressive. Thus, higher senescence rates in males and white-striped birds would support the intra-sexual competition hypothesis, whereas higher senescence rates in females and tan-striped birds would support the parental investment hypothesis. White-striped males showed the lowest rate of actuarial senescence. Tan-striped females had the highest senescence rate, and tan-striped males and white-striped females showed intermediate, relatively equal rates. Thus, results were inconsistent with sexual selection and competitive strategies increasing senescence rates, and instead indicate that senescence may be accelerated by female-biased parental care, and lessened by sharing of parental duties.

Abstract. Females from polymorphic species could theoretically benefit by adjusting offspring morph composition, since morphs often differ in ecological and behavioral traits, and may be differentially susceptible to environmental conditions. Although offspring sex ratio adjustments have been increasingly supported, whether, and in which contexts, genetically determined morph ratios are adjusted has not been established. We used a long-term dataset to examine whether broad-scale climatic patterns characterized by teleconnection indices, population composition, and other environmental factors affect offspring sexmorph ratios in the white-throated sparrow (Zonotrichia albicollis), a species with chromosomal morph determination. We predicted that females might overproduce the underrepresented sex or morph, since pairing is disassortative by morph, and might also produce more white morph male offspring given favorable climatic conditions, because white males (WMs) are large, promiscuous, and expensive to produce. The proportion of WM-by-tan female breeding pairs and recruitment of WMs declined following winters with high Pacific North American teleconnection indices, and females of both morphs produced more WM offspring after these relatively cold winters. These winters and the following springs were also associated with low Southern Oscillation indices, indicating El Niño. Females of both morphs also produced fewer males late in asynchronously hatching broods. Adjustment of brood composition in response to climatically mediated changes in population composition could stabilize the white-throated sparrow's disassortative breeding system and genetic polymorphism.