Rapid speciation via the evolution of pre-mating isolation in the Ibera Seedeater
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Choosy females drive isolation

Rapid radiations of recently diverged species represent an excellent opportunity for exploring drivers of speciation. The capuchino seedeaters, a group of South American birds, include a number of species that, in the field, are often discernable only through male plumage and song. Turbek et al. used genomes and behavioral experiments to identify potential isolating factors in two members of this group and found that, though entirely sympatric, females mated only with conspecific males and that only a few genes differed between the species (see the Perspective by Jarvis). Thus, a small reshuffling of genes and reinforcement through mate choice has driven divergence in these overlapping and very similar species.

Science, this issue p. eabc0256; see also p. 1312

Structured Abstract

INTRODUCTION

Organisms in the early stages of speciation provide an opportunity to understand the processes that govern reproductive isolation between taxa. Ecological or behavioral mechanisms can serve as powerful barriers to the interbreeding of co-occurring species at the onset of their divergence. Tracking mating decisions within wild populations early in speciation can improve our understanding of how behavioral isolation promotes divergence.

RATIONALE

The southern capuchino seedeaters (Sporophila) are one of the most rapid avian radiations, showing remarkably low ecological and genomic divergence. We took advantage of the recent discovery of a capuchino species, the Iberá Seedeater (S. iberaensis), to study the origin and importance of pre-mating barriers early in speciation. By combining genomic and behavioral analyses, we examined (i) the role of assortative mating in the maintenance of species boundaries, (ii) the phenotypic traits underlying species recognition, (iii) the genomic basis of such traits, and (iv) the origin of these genomic variants.

RESULTS

Sporophila iberaensis was first observed in 2001 and co-occurs with S. hypoxantha throughout its main breeding location in the northern portion of the Iberá wetlands of Argentina. Across two breeding seasons, we located nests and collected genomic samples from both species. We found extremely low genome-wide differentiation, with the exception of three narrow regions located on different chromosomes. These regions contained 12 genes, three of which are involved in plumage coloration (TYRP1, OCA2, and HERC2). Sporophila hypoxantha and S. iberaensis males differ in coloration and song, but females are indistinguishable in coloration across the avian visual spectrum. We therefore used genomic data to quantify assortative mating. Each female’s species-specific genotype always matched the genotype of her mate, demonstrating strong assortative mating despite these two species holding neighboring breeding territories, breeding synchronously, and foraging together on the same grasses. We tested the importance of divergent plumage patterning and song in species recognition and pre-mating isolation through playback experiments in the field. We presented territorial males with combinations of conspecific and heterospecific song and plumage, and assessed their aggressive behavioral responses. Each species responded most aggressively to conspecific song and plumage, confirming that both traits are used to recognize sexual competitors. Finally, we investigated the origin of the novel S. iberaensis plumage phenotype by examining genomic differentiation across the broader capuchino radiation. Although multiple species shared variants with S. iberaensis in the areas of elevated differentiation, the specific combination of these variants across the divergent regions distinguished S. iberaensis from all other capuchinos.

CONCLUSION

Our findings point to pre-mating isolation through assortative mate choice, based on both plumage coloration and song, as a primary mechanism promoting divergence between these co-occurring capuchino species. Although the ultimate fate of the incipient S. iberaensis species remains uncertain, our findings illustrate how lineages can form and quickly become reproductively isolated from co-occurring, syntopic species. Our results further suggest that the reshuffling of existing genetic variation can generate novel phenotypes that are then targeted by sexual selection. Assortative mating based on these traits may maintain species boundaries early in speciation while subsequent reproductive barriers accumulate.

Novel mating signals restrict gene flow between co-occurring bird species.

Sporophila iberaensis was first observed in 2001 and has a breeding range contained entirely within that of S. hypoxantha. Despite extremely low genomic differentiation, both species mate assortatively. Genetic differentiation is concentrated near genes known to be involved in plumage coloration. Field experiments show that both song and plumage are used to recognize sexual competitors.

” data-hide-link-title=”0″ data-icon-position=”” href=”https://science.sciencemag.org/content/sci/371/6536/eabc0256/F1.large.jpg?width=800&height=600&carousel=1″ rel=”gallery-fragment-images-1434066126″ title=”Novel mating signals restrict gene flow between co-occurring bird species. Sporophila iberaensis was first observed in 2001 and has a breeding range contained entirely within that of S. hypoxantha. Despite extremely low genomic differentiation, both species mate assortatively. Genetic differentiation is concentrated near genes known to be involved in plumage coloration. Field experiments show that both song and plumage are used to recognize sexual competitors.”>

Novel mating signals restrict gene flow between co-occurring bird species.

Sporophila iberaensis was first observed in 2001 and has a breeding range contained entirely within that of S. hypoxantha. Despite extremely low genomic differentiation, both species mate assortatively. Genetic differentiation is concentrated near genes known to be involved in plumage coloration. Field experiments show that both song and plumage are used to recognize sexual competitors.

Abstract

Behavioral isolation can catalyze speciation and permit the slow accumulation of additional reproductive barriers between co-occurring organisms. We illustrate how this process occurs by examining the genomic and behavioral bases of pre-mating isolation between two bird species (Sporophila hypoxantha and the recently discovered S. iberaensis) that belong to the southern capuchino seedeaters, a recent, rapid radiation characterized by variation in male plumage coloration and song. Although these two species co-occur without obvious ecological barriers to reproduction, we document behaviors indicating species recognition by song and plumage traits and strong assortative mating associated with genomic regions underlying male plumage patterning. Plumage differentiation likely originated through the reassembly of standing genetic variation, indicating how novel sexual signals may quickly arise and maintain species boundaries.

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