RESUMO
The effects of genetic introgression on species boundaries and how they affect species' integrity and persistence over evolutionary time have received increased attention. The increasing availability of genomic data has revealed contrasting patterns of gene flow across genomic regions, which impose challenges to inferences of evolutionary relationships and of patterns of genetic admixture across lineages. By characterizing patterns of variation across thousands of genomic loci in a widespread complex of true toads (Rhinella), we assess the true extent of genetic introgression across species thought to hybridize to extreme degrees based on natural history observations and multilocus analyses. Comprehensive geographic sampling of five large-ranged Neotropical taxa revealed multiple distinct evolutionary lineages that span large geographic areas and, at times, distinct biomes. The inferred major clades and genetic clusters largely correspond to currently recognized taxa; however, we also found evidence of cryptic diversity within taxa. While previous phylogenetic studies revealed extensive mitonuclear discordance, our genetic clustering analyses uncovered several admixed individuals within major genetic groups. Accordingly, historical demographic analyses supported that the evolutionary history of these toads involved cross-taxon gene flow both at ancient and recent times. Lastly, ABBA-BABA tests revealed widespread allele sharing across species boundaries, a pattern that can be confidently attributed to genetic introgression as opposed to incomplete lineage sorting. These results confirm previous assertions that the evolutionary history of Rhinella was characterized by various levels of hybridization even across environmentally heterogeneous regions, posing exciting questions about what factors prevent complete fusion of diverging yet highly interdependent evolutionary lineages.
Uma atenção crescente tem sido dada aos efeitos da introgressão genética nos limites das espécies e como eles afetam a integridade e a persistência das espécies ao longo do tempo evolutivo. A crescente disponibilidade de dados genômicos revelou padrões contrastantes de fluxo gênico entre regiões do genoma, o que impõe desafios às inferências de relações evolutivas e de padrões de mistura genética entre linhagens. Com base em padrões de variação em milhares de marcadores genômicos em um complexo amplamente distribuído de sapos (Rhinella), avaliamos a extensão de introgressão genética entre espécies que, acredita-se, hibridizam amplamente com base em observações de história natural e análises multi-locus. Nossa amostragem geográfica abrangente de cinco táxons neotropicais revelou várias linhagens evolutivas distintas que abrangem grandes áreas geográficas e, por vezes, biomas distintos. Os principais clados e grupos genéticos inferidos correspondem em grande parte aos táxons atualmente reconhecidos; no entanto, também encontramos evidência de diversidade críptica. De acordo com estudos filogenéticos anteriores que revelaram extensa discordância mitonuclear, nossas análises de agrupamento genético revelaram vários indivíduos geneticamente misturados. Adicionalmente, análises demográficas históricas sugerem que a história evolutiva desses sapos envolveu fluxo gênico entre táxons tanto em épocas antigas quanto recentes. Por fim, testes ABBA-BABA revelaram amplo compartilhamento de alelos entre espécies, um padrão que pode ser atribuído à introgressão genética ao invés de sorteamento incompleto de alelos entre linhagens. Esses resultados confirmam sugestões anteriores de que a história evolutiva de Rhinella foi caracterizada por vários níveis de hibridização, mesmo entre ambientes distintos, levantando questões sobre quais fatores impedem a fusão completa de linhagens evolutivas divergentes porém altamente interdependentes.
Assuntos
Bufonidae , Fluxo Gênico , Hibridização Genética , Alelos , Animais , Bufonidae/genética , Demografia , Filogenia , América do SulRESUMO
Mitonuclear discordance is a frequently encountered pattern in phylogeographic studies and occurs when mitochondrial and nuclear DNA display conflicting signals. Discordance among these genetic markers can be caused by several factors including confounded taxonomies, gene flow, and incomplete lineage sorting. In this study, we present a strong case of mitonuclear discordance in a species complex of toads (Bufonidae: Incilius coccifer complex) found in the Chortís Block of Central America. To determine the cause of mitonuclear discordance in this complex, we used spatially explicit genetic data to test species limits and relationships, characterize demographic history, and quantify gene flow. We found extensive mitonuclear discordance among the three recognized species within this group, especially in populations within the Chortís Highlands of Honduras. Our data reveal nuclear introgression within the Chortís Highlands populations that was most probably driven by cyclical range expansions due to climatic fluctuations. Though we determined introgression occurred within the nuclear genome, our data suggest that it is not the key factor in driving mitonuclear discordance in the entire species complex. Rather, due to a lack of discernible geographic pattern between mitochondrial and nuclear DNA, as well as a relatively recent divergence time of this complex, we concluded that mitonuclear discordance has been caused by incomplete lineage sorting. Our study provides a framework to test sources of mitonuclear discordance and highlights the importance of using multiple marker types to test species boundaries in cryptic species.