Biogeographic history of S. corvina
Based on our results and previous work on the genus Sporophila , we suggested a possible biogeographic scenario that explains the distribution, divergence, and patterns of gene flow between subspecies of S. corvina . The radiation of the genus of Sporophilaseedeaters was initiated around the late Miocene to early Pliocene in South America, followed by multiple independent bouts of colonization of Middle America (Mason & Burns, 2013; Mason et al., 2018; Ocampo et al., 2022a). The ancestral population of the S. corvina likely diverged from the S. intermedia ancestor, in the late Pliocene, after a trans-Andes dispersion event (Ocampo et al., 2022a; Stiles, 1996), and dispersed northwards through the Panamanian isthmus (O’Dea et al., 2016). At this time, the Talamanca mountain range was already formed to its current elevation (Coates & Obando, 1996), thus imposing a barrier to lowland bird species. Therefore, the ancestral S. corvina population likely dispersed through the Pacific and Caribbean slopes, around the Talamanca mountain range. The population moving north of Talamanca likely passed through the wetter Caribbean slope reaching higher latitudes. This all-black lineage may have been isolated (Figure 2B) due to habitat fragmentation associated with forest expansion and contraction events, as well as wet and arid environmental conditions associated with climate oscillations during the Pleistocene (e.g., Garzón-Orduña et al., 2014). On the other hand, the population south of the Talamanca mountain range reached a boundary that prevented it from moving farther north – an ecological and geological boundary known as the “Tarcoles Line” (Kohlmann & Wilkinson, 2007). This ecotone separates the tropical wet forest of the Costa Rican South Pacific and Middle American dry forest, and constrains the distribution of many species (Kohlmann & Wilkinson, 2007), and is likewise largely consistent with the current limit of the subspecies range of S. c. hoffmanni .
Based on this biogeographic scenario, gene flow during secondary contact between clades, associated with most recent periods of population expansion, resulted in the currently continuous distribution of S. c. hoffmanni and S. c. hicksii and the introgression fromS. c. corvina into S. c. hicksii at the Canal in central Panama. More recently, secondary contact was established in the Central Valley of Costa Rica, likely favored by deforestation due to human urban expansion (Biamonte et al., 2011; Joyce, 2006). We found no evidence of current hybridization between these two subspecies in the Central Valley region (Figures 3 and 4; Table 3). However, the strength of reproductive isolation is dynamic, and premating reproductive barriers vary with time since contact. Reproductive barriers can increase after secondary contact due to sexual characters displacement (e.g., Jaya et al., 2022), or the initial reduced gene flow after secondary contact can increase with time since contact, favoring hybridization and resulting in the merger of distinct populations (Bettles et al., 2005). Further behavioral studies in the Central Valley region could provide insights on the factors maintaining reproductive isolation between subspecies at the early stages of secondary contact.
CONCLUSIONS
Sporophila corvina from Costa Rica and Panama form three genetically differentiated groups that are largely consistent with their current subspecies classifications and geographic distributions. The three subspecies have established three different contact zones and hybridize extensively across two of them, regardless of the differences in plumage patterns of the populations that came into contact (pied vs. pied or black vs. pied). However, even though plumage divergence does not act as a strong barrier to gene flow, we found that plumage traits are divergent and presumably under selection at the contact zones. Finally, model-based demographic inference suggests that the black subspecies S. c. corvina diverged in isolation until a recent secondary contact with S. c. hicksii, resulting in the hybridization pattern that we see today at one of these contact zones. Overall, our results suggest that divergence in plumage color is important in reducing gene flow between these populations, but not sufficient to stablish complete reproductive isolation. Other factors, such as reproductive timing or divergence in song, might explain why hybridization is reduced in one of the contact zones but not in the others, a pattern of isolation that is likely to change with time.
ACKNOWLEDGMENTS
We thank The University of Alaska Museum, Louisiana State University, Universidad de Costa Rica, and Smithsonian Tropical Research Institute collections and their personnel for providing tissue samples used in this study; SINAC in Costa Rica, and MIAMBIENTE in Panama for granting research permits; McMillan O., Amador S., Lopez O., STRI’s personnel, Arce A., Biamonte E., Morrison O., Sánchez C., and Barrantes G. for assistance and logistical support in Costa Rica and Panama; CIRC (UR) for access to computing facilities; Searcy W., Campagna, L., the Mason lab (LSU), and the Uy lab (UR) for valuable comments that improved early versions of the manuscript; Lastly, we thank our funding sources, the University of Rochester’s Global Visitor Program (College of Arts and Sciences), the Hesse student award from the American Ornithological Society, the Short-term fellowship from the Smithsonian Tropical Research Institute, and the Kushlan and Savage funds from the University of Miami (to D. Ocampo), and the Aresty Chair in Tropical Ecology from the University of Miami (to J.A.C. Uy).
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DATA AVAILABILITY STATEMENT
SNPs and phenotypic data are available on Dryad data repository (Ocampo et al., 2022b). “Scorvina_SNPs_1.vcf” and “Scorvina_SNPs_2.vcf” contain the SNPs data sets according to our two filtering criteria. “Scorvina_B2.txt” including plumage brightness per patch per individual. “Scorvina_morph.txt” including morphometric data. Related metadata can be found in Table S1 (including georeferences in decimal degrees and date/month/year of sampling event).
BENEFIT-SHARING STATEMENT
Benefits Generated: A collaborative research was developed with scientists and institutions providing genetic samples, all collaborators are included as co-authors. Other contributors to the research are included in the ACKNOWLEDGEMENTS section. The results of the research have been shared with the scientific community.
AUTHOR CONTRIBUTIONS
D. Ocampo and A. Uy conceptualized the study; D. Ocampo, K. Winker, M. Miller, and L. Sandoval collected the samples; D. Ocampo collected phenotypic data and performed data analyses. D. Ocampo and A. Uy drafted the manuscript with significant input of all authors. All authors have read and approved the final manuscript.