Kay, K. M. | bioRxiv Science

bioRxiv2026

Divergent habitat selection across many loci maintains species boundaries during introgression

Evidence of introgression between well-defined species is abundant, begging the question, how are species boundaries maintained during introgression? Work on this question has largely focused on systems where divergence is controlled by a few large effect genetic loci. However, adaptive divergence is often highly polygenic, especially between young species that remain capable of gene exchange. Here, we use phylogeny based introgression statistics and local ancestry inference to characterize the genomic, spatial, and historical extent of introgression between two recently diverged Neotropical plant species. We then use QTL analysis to investigate the genetic basis of traits under divergent abiotic and biotic selection that are involved in habitat isolation. Finally, we combine these top-down and bottom-up approaches to clarify how species with polygenic reproductive isolation maintain cohesion in the face of gene flow. We find clear evidence of both recent and ancient introgression between Costus villosissimus and C. allenii, but overall genomic divergence remains relatively high (Fst:[~] 0.27) in part due to strong divergent habitat selection. Traits involved in divergent habitat adaptation are polygenic, such that strong habitat selection is spread across many loci rather than concentrated on a few loci of large effect. In contrast to the islands of divergence seen around large effect loci in other hybridizing species pairs, we see genomically widespread and moderate peaks of both differentiation and introgression. Our results indicate that strong selection spread across many loci contributing to reproductive isolation can maintain species differentiation despite introgression. Significance StatementGene flow between species (introgression) reduces genetic differentiation. And yet, introgression between well-defined species is common. How do species remain distinct in the face of introgression? Previous work focuses on differentiation maintained by elevated divergence in a few genomic regions (loci) with large effects. However, many loci with small effects commonly control differences between species. To clarify how species with abundant differentiating loci can remain distinct during introgression, we described patterns of introgression between two Neotropical plants and characterized the genetic basis of their divergent habitat adaptation. We found that isolation by divergent habitat adaptation is likely controlled by numerous small-effect and genomically widespread loci, and that habitat selection across multiple traits is sufficient to maintain differentiation despite ongoing introgression.

evolutionary biology↗

bioRxiv2024

Repeated loss of floral scent in independent transitions from bee to hummingbird pollination in spiral gingers

The repeated evolution of the same trait in different lineages provides powerful natural experiments to study the phenotypic and genotypic predictability of how traits are gained and lost. A fascinating example of this is the repeated evolution of hummingbird pollination in plant lineages in the Americas, a widespread and often unidirectional phenomenon. The spiral gingers in the genus Costus are ancestrally bee-pollinated, and hummingbird pollination has evolved multiple times independently in the tropical Americas. These pollinator transitions are accompanied by predictable morphological and color changes, but the changes in floral scent have not been described. In this study, we describe the floral scent composition of 30 species of Costus sampled across the phylogeny to understand how floral scent has evolved across the genus with respect to pollinator transitions. We then combine transcriptomics and genomics to identify genetic expression differences and gene family evolution associated with pollinator transitions. We show that hummingbird-pollinated species have mostly lost their floral scent, whereas bee-pollinated species exhibit either floral scent maintenance or in some cases, gains of more diverse scent profiles. We find the floral scent loss appears to be due to gene downregulation rather than pseudogenization. The remarkable consistency of scent loss in hummingbird-pollinated species highlights the shared strong selection pressures experienced by these lineages. Even species with more recent transitions from bee to hummingbird pollination exhibit scent loss, highlighting the rapid breakdown of scent production following pollinator transitions. This research highlights the capacity for rapid changes when selection pressures are strong through downregulation of floral scent genes. ResumenLa evolucion independiente de un rasgo en diferentes linajes ofrece la oportunidad de estudiar la predictibilidad de fenotipos y sus bases geneticas. Un ejemplo fascinante es la evolucion repetida de polinizacion por colibries en varios linajes de plantas en las Americas, un fenomeno generalizado y tipicamente unidireccional. Las especies de cana agria del genero Costus son polinizadas ancestralmente por abejas y la polinizacion por colibries ha evolucionado varias veces de forma independiente en America tropical. Cada transicion de polinizador ha sido acompanada de varios cambios morfologicos y colores predecibles, pero los cambios en el aroma floral no han sido descritos. En este estudio describimos la composicion del aroma floral de 30 especies de Costus para comprender como el aroma floral ha evolucionado con respecto a las transiciones de polinizadores. Combinamos transcriptomica y genomica en un clado de Costus para identificar diferencias en la expresion genetica y la evolucion de la familia de genes asociadas con las transiciones de polinizadores. Nuestros resultados muestran que las especies polinizadas por colibries han perdido en su mayoria su aroma floral, mientras que las especies polinizadas por abejas ya sea mantienen el aroma floral y, en algunos casos, muestran ganancias de perfiles de aroma mas diversos. La consistencia en la perdida de olor en especies polinizadas por colibries resalta las fuertes presiones de seleccion natural que experimentan estos linajes. Incluso las especies con transiciones mas recientes de polinizacion de abejas a colibries exhiben perdida de olor, lo que destaca la rapida interrupcion de la produccion de olores despues de las transiciones de los polinizadores. Tambien encontramos que la perdida de aroma floral parece estar controlada por regulacion genica negativa y no por la perdida de genes de produccion de aromas (e.g. pseudogenizacion). Esta investigacion destaca la rapidez de cambios a traves de la regulacion negativa de genes que controlan aromas florales cuando las presiones de seleccion son fuertes. Significance StatementThe independent evolution of the same trait in different lineages provides a natural experiment to investigate the predictability of evolution. A fascinating example is the evolution of hummingbird pollination, which has occurred many times across flowering plants, and often involves convergence in multiple traits. In this study, we combine comparative chemical ecology with genomics and transcriptomics to study floral scent evolution in the genus Costus. We show that species exhibit loss of floral scent following transitions to hummingbird pollination suggesting a shared strong selection pressure favoring scent loss. We demonstrate the floral scent loss appears to be due to gene downregulation. This research highlights the capacity for rapid changes when selection pressures are strong through downregulation of scent genes.

evolutionary biology↗

bioRxiv2020

Patterns of speciation are similar across mountainous and lowland regions for a Neotropical plant radiation (Costaceae: Costus)

High species richness and endemism in tropical mountains are recognized as major contributors to the latitudinal diversity gradient. The processes underlying mountain speciation, however, are largely untested. The prevalence of steep ecogeographic gradients and the geographic isolation of populations by topographic features are predicted to promote speciation in mountains. We evaluate these processes in a species-rich Neotropical genus of understory herbs that range from the lowlands to montane forests and have higher species richness in topographically complex regions. We ask whether climatic niche divergence, geographic isolation, and pollination shifts differ between mountain-influenced and lowland Amazonian sister pairs inferred from a 756-gene phylogeny. Neotropical Costus ancestors diverged in Central America during a period of mountain formation in the last 3 My with later colonization of Amazonia. Although climatic divergence, geographic isolation, and pollination shifts are prevalent in general, these factors dont differ between mountain-influenced and Amazonian sister pairs. Despite higher climatic niche and species diversity in the mountains, speciation modes in Costus appear similar across regions. Thus, greater species richness in tropical mountains may reflect differences in colonization history, diversification rates, or the prevalence of rapidly evolving plant life forms, rather than differences in speciation mode.

evolutionary biology↗