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Abstract In song-learning birds, vocalizations are species recognition signals and may act as premating reproductive barriers; for allopatric taxa, testing how the signals can influence the speciation processes is quite challenging. This study aims to understand genomic divergence and species recognition via songs in 2 allopatric taxa, eastern and western Nashville warblers (Leiothlypis ruficapilla ruficapilla vs. Leiothlypis ruficapilla ridgwayi). We performed playback experiments to assess their reciprocal behavioral responses, which suggests an asymmetric barrier: the eastern L. r. ruficapilla discriminates between the 2 songs, but the western L. r. ridgwayi does not. Using whole-genome sequencing, we also examined the extent of the taxa’s genomic divergence and estimated their demographic history. We identified dozens of highly differentiated genomic regions, as well as fluctuations in historical effective population sizes that indicate independent demographic trajectories during the Pleistocene. To contextualize the magnitude of divergence between L. ruficapilla subspecies, we applied the same genomic analyses to 2 additional eastern-western pairs of parulid warblers, Setophaga virens vs. Setophaga townsendi and Setophaga coronata coronata vs. Setophaga coronata auduboni, which have existing behavior studies but are not in strict allopatry. Our findings provide insights into the role of vocalizations in defining within-pair relationship and the important legacy of isolation during the Pleistocene. 

Abstract The search for the genetic basis of phenotypes has primarily focused on single nucleotide polymorphisms, often overlooking structural variants (SVs). SVs can significantly affect gene function, but detecting and characterizing them is challenging, even with long-read sequencing. Moreover, traditional single-reference methods can fail to capture many genetic variants. Using long reads, we generated a Capuchino Seedeater (Sporophila) pangenome, including 16 individuals from 7 species, to investigate how SVs contribute to species and coloration differences. Leveraging this pangenome, we mapped short-read data from 127 individuals, genotyped variants identified in the pangenome graph, and subsequently performed FST scans and genome-wide association studies. Species divergence primarily arises from SNPs and indels (< 50 bp) in non-coding regions of melanin-related genes, as larger SVs rarely overlap with divergence peaks. One exception was a 55 bp deletion near the OCA2 and HERC2 genes, associated with feather pheomelanin content. These findings support the hypothesis that the reshuffling of small regulatory alleles, rather than larger species-specific mutations, accelerated plumage evolution leading to prezygotic isolation in Capuchinos. 

Abstract Populations expanding their ranges experience unique evolutionary dynamics, with perhaps the most ubiquitous being an increased role for genetic drift. The increase in genetic drift during range expansion is predicted to increase the frequency of deleterious alleles along the expansion edge, termed expansion load, and therefore reduce fitness at the edge of expansions. While theoretical predictions of expansion load are well established, direct links between whole-genome estimates of load and decreases in an expanding population’s fitness remain scarce. We quantified expansion load during experimental range expansions of the red flour beetle (Tribolium castaneum) and then regressed observed population growth rates against estimated genetic loads to characterize if and how much expansion load decreased fitness at expansion edges. As predicted by theory, gene surfing resulted in the fixation of an increased number of putatively deleterious alleles. However, metrics of whole-genome load displayed relatively weak relationships with fitness. We suggest this discrepancy may partly be due to the recessive nature of some deleterious variation, which our data were not able to robustly assess. Genetic diversity, in contrast, was strongly associated with fitness and may provide a robust, easy-to-assess metric for expanding populations. 

Abstract The persistence of polymorphisms in aposematic species remains one of the most interesting paradoxes in evolutionary biology because aposematism theory suggests that polymorphisms should be unstable over time. We offer an explanation for the persistence of aposematic polymorphisms that considers not only the role of natural selection but also the role of sexual selection. While predation and mate choice generally act to erode signal variation, intraspecific competition may facilitate polymorphisms by reducing mate competition for males bearing the rarer warning signal. We tested this hypothesis in a population of the strawberry poison frog (Oophaga pumilio), where red (common) and yellow (rare) morphs coexist using (1) a 10-year capture–mark–recapture experiment to study natural selection, (2) a territorial intrusion experiment, and (3) previously published mate choice experiments to study sexual selection. We found that rare yellow males suffer less aggression from male conspecifics, suggesting negative frequency dependent selection. Moreover, the more common and choosier red females have lower apparent survival than their less choosy yellow counterparts, suggesting that survival may be better explained by costs of exercising mate choice rather than by predation. Our work highlights the importance of considering multiple sources of selection in explaining the paradoxical persistence of aposematic polymorphisms. 

Abstract The establishment of reproductive isolation between species via gametic incompatibility initially requires within-species variation in reproductive compatibility. We investigate how within-species variation in sperm and egg recognition proteins, potentially generated via sexual conflict, influences reproductive isolation between two partially sympatric sea urchin species; the North American west coast Mesocentrotus franciscanus and the circumpolar Strongylocentrotus droebachiensis. Barriers to hybridization are stronger when eggs are given a choice of conspecific versus heterospecific sperm and the variation in hybridization among crosses can be explained by whether the sperm or egg protein variant is ancestral or derived. Derived proteins can be recognized as different and prevent hybridization. Examination of the allele frequencies of these proteins in M. franciscanus in and out of sympatry with S. droebachiensis along the west coast of North America reveals evidence of reinforcement selection and reproductive character displacement in eggs but not sperm, which likely reflects the differential cost of hybridization for males and females. 

Abstract Traits that have lost function sometimes persist through evolutionary time. Persistence may occur if there is not enough standing genetic variation for the trait to allow a response to selection, if selection against the trait is weak relative to drift, or if the trait has a residual function. To determine the evolutionary processes shaping whether nonfunctional traits are retained or lost, we investigated short stamens in 16 populations of Arabidopsis thaliana along an elevational cline in northeast Spain. A. thaliana is highly self-pollinating and prior work suggests short stamens do not contribute to self-pollination. We found a cline in short stamen number from retention of short stamens in high-elevation populations to incomplete loss in low-elevation populations. We did not find evidence that limited genetic variation constrains short stamen loss at high elevations, nor evidence for divergent selection on short stamens between high and low elevations. Finally, we identified loci associated with short stamens in northeast Spain that are different from loci associated with variation in short stamens across latitudes from a previous study. Overall, we did not identify the evolutionary mechanisms contributing to an elevational cline in short stamen number so further research is clearly warranted. 

Abstract Understanding how the early stages of sexual signal diversification proceed is critically important because these microevolutionary dynamics directly shape species trajectories and impact macroevolutionary patterns. Unfortunately, studying this is challenging because signals involve complex interactions between behavior, morphology, and physiology, much of which can only be measured in real-time. In Hawaii, male Pacific field cricket song attracts both females and a deadly parasitoid fly. Over the past two decades, there has been a marked increase in signal variation in Hawaiian populations of these crickets, including novel male morphs with distinct mating songs. We capitalize on this rare opportunity to track changes in morph composition over time in a population with three novel morphs, investigating how mate and parasitoid attraction (components of sexual and natural selection) may shape signal evolution. We find dramatic fluctuation in morph proportions over the three years of the study, including the arrival and rapid increase of one novel morph. Natural and sexual selection pressures act differently among morphs, with some more attractive to mates and others more protected from parasitism. Collectively, our results suggest that differential protection from parasitism among morphs, rather than mate attraction, aligns with recent patterns of phenotypic change in the wild. 

Abstract Theory predicts that thermal developmental plasticity evolves in response to thermal heterogeneity, suggesting that plasticity may be an important trait for establishment in novel climates. However, few studies use multispecies comparisons to examine how plasticity evolves, meaning that there is little empirical basis with which to examine key theoretical predictions. We estimate patterns of thermal developmental plasticity in morphological and performance traits for 7 Anolis lizard species inhabiting South Florida, USA. We found interspecific differences as well as intraspecific variation in reaction norms across species. Neither temperature heterogeneity in present-day invasive ranges in Florida nor historical temperature heterogeneity from the contemporary native ranges predicted reaction norm variation. Phylogeny and species identity typically predicted around 90%–95% of reaction norm variation. Overall, these results suggest that thermal developmental plasticity in these traits exhibits variation that could be inconsistent with patterns expected under adaptive evolution to macroclimate. Examining the role of maternal nesting behavior and sampling of additional species can help to distinguish between neutral variation and selection toward multiple adaptive peaks. Our comparative study of thermal developmental plasticity in lizards provides new insights about macroevolutionary dynamics behind the evolution of developmental plasticity and the conditions under which adaptive plasticity is expected to evolve. 

Abstract Sexual dichromatism is thought to evolve primarily as a function of sexual selection, especially female choice. However, other forces, from sex-specific environmental conditions to social signaling in females, can also generate color differences between sexes. We studied dewlap dichromatism across 292 species of Anolis lizards. Dewlaps are colorful throat ornaments found on males of most anole species but are also present in females in many species. Although male and female dewlaps often have similar coloration, in some species, they are strikingly dichromatic. We found that ornament color is labile and that dichromatism results from the loss of costly pigments in females. This pattern could indicate a shift towards signal loss in females; however, the secondary gains of female dewlaps across the phylogeny suggest a potential advantageous function. Possible mechanisms for female dewlap coloration include social selection, nonsexual signaling, or detectability in different microhabitats (e.g., sensory drive). Female dewlap color overlap between co-occurring species is both less than expected by chance overall and reduced in species-rich communities, suggesting that dichromatism could be driven by competition. Our results highlight that selection on females drives the observed pattern of dichromatism, suggesting a potentially adaptive role for female ornaments and emphasizing the need for additional work to understand female ornament evolution. 

Abstract Parallel evolution of the same reproductive isolation barrier within a taxon is an indicator of ecology’s role in speciation (i.e., parallel speciation), yet spatiotemporal variability in the efficacy of the barrier can present challenges to retracing how it evolved. Here, we revisit the evidence for a candidate example of parallel speciation in a clade of scincid lizards (the Plestiodon skiltonianus complex) using genomic data, with emphasis on determining whether hybridization may have confounded the phylogenetic signals of parallelism for this group. Our results show a striking case of genealogical discordance, in which mitochondrial loci support multiple origins of a derived large-bodied morphotype (Plestiodon gilberti) within a small-bodied ancestor (Plestiodon skiltonianus), whereas nuclear loci indicate a single origin. We attribute the discordance to separate, temporally-spaced hybridization events that led to asymmetric capture of P. skiltonianus mitochondria in different regional lineages of P. gilberti. Nuclear introgression showed a similar directional bias but was less pervasive. We demonstrate how a mechanical reproductive barrier previously identified for this group explains the asymmetry of mitochondrial introgression, given that hybrid matings are most likely when the male is P. gilberti and the female is P. skiltonianus. We then use permutation tests of morphological data to provide evidence that the mechanical barrier is less stringent in areas where hybridization is inferred to have occurred. Our results demonstrate how biased hybridization can dictate which genetic variants are transmitted between species and emphasize the importance of accounting for introgression and deep coalescence in identifying phyletic signatures of parallel speciation.