From micro- to macroevolution: insights from a Neotropical bromeliad with high population genetic structure adapted to rock outcrops

Abstract

Geographic isolation and reduced population sizes can lead to local extinction, low efficacy of selection and decreased speciation. However, population differentiation is an essential step of biological diversification. In allopatric speciation, geographically isolated populations differentiate and persist until the evolution of reproductive isolation and ecological divergence completes the speciation process. Pitcairnia flammea allows us to study the evolutionary consequences of habitat fragmentation on naturally disjoint rock-outcrop species from the Brazilian Atlantic Rainforest (BAF). Our main results showed low-to-moderate genetic diversity within populations, and deep population structuring caused by limited gene flow, low connectivity, genetic drift and inbreeding of long-term isolation and persistence of rock-outcrop populations throughout Quaternary climatic oscillations. Bayesian phylogenetic and model-based clustering analyses found no clear northern and southern phylogeographic structure commonly reported for many BAF organisms. Although we found two main lineages diverging by ~2 Mya during the early Pleistocene, species' delimitation analysis assigned most of the populations as independent evolving entities, suggesting an important role of disjoint rock outcrops in promoting high endemism in this rich biome. Lastly, we detected limited gene flow in sympatric populations although some hybridization and introgression were observed, suggesting a continuous speciation process in this species complex. Our data not only inform us about the extensive differentiation and limited gene flow found among Pitcairnia flammea species complex, but they also contain information about the mechanisms that shape the genetic architecture of small and fragmented populations of isolated rock outcrop of recently radiated plants.

Genome Skimming Reveals Widespread Hybridization in a Neotropical Flowering Plant Radiation

“…In these cases, the interaction between multiple reproductive barriers such as different reproductive systems, variation in floral traits, temporal flowering differences and low hybrid seed viability may have limited interspecific crosses and helped to maintain species integrity (Zanella et al, 2016;Neri et al, 2017). Similar results have been found in other genera such as Pitcarnia (Palma-Silva et al, 2011;Mota et al, 2020). However, these studies were done at the population level and explicitly targeted recent or ongoing gene-flow within small sympatric populations, whereas we focused on the longterm evolutionary signature of introgression across the whole subfamily.…”

“…Aechmea (Goetze et al, 2017), Alcantarea (Versieux et al, 2012;Lexer et al, 2016), Fosterella (Paule et al, 2017), Pitcairnia (Palma-Silva et al, 2011Mota et al, 2020), Puya (Jabaily and Sytsma, 2010;Schulte et al, 2010), Tillandsia (Gardner, 1984;Gonçalves and de Azevêdo-Gonçalves, 2009), and Vriesea (Matos et al, 2016;Zanella et al, 2016;Neri et al, 2018). Despite this wealth of evidence for a strong hybridization potential in bromeliads, population genetic studies generally have found low levels of interspecific gene flow in extant populations of bromeliads.…”

Underlying microevolutionary processes parallel macroevolutionary patterns in ancient neotropical mountains

“…Accordingly, diversification events throughout the Quaternary are congruent amongst many extant lineages from distinct Neotropical montane formations, as in the Espinhaço itself (e.g. Barres et al, 2019;Bonatelli et al, 2014;Chaves et al, 2019;Nascimento et al, 2018;Vasconcelos et al, 2020); Serra do Mar and Mantiqueira mountains (Mota et al, 2020); the páramos (e.g. Hughes & Atchison, 2015;Madriñán et al, 2013) and the pantepuis (e.g.…”

“…In fact, restricted population connectivity has been reported for several naturally fragmented habitats, especially in mountain systems (e.g. Mota et al, 2020;Muellner-Riehl et al, 2019). Such limited gene flow amongst populations suggests that both pollen and seed dispersal might be restricted.…”

Taxon-specific or universal? Using target capture to study the evolutionary history of rapid radiations

“…Here, we present Bromeliad1776, a new bait set for targeted sequencing, designed to address a wide range of evolutionary hypotheses in Bromeliaceae: from producing robust phylogenies to studying the interplay of genomic processes during speciation and the genetic basis of trait shifts, such as photosynthetic and pollination syndrome. This highly diverse Neotropical radiation provides an excellent research system for studying the drivers and constraints of rapid adaptive radiation (Benzing, 2000;Givnish et al, 2011;Loiseau et al, 2021;Mota et al, 2020;Palma-Silva & Fay, 2020;Wöhrmann, Michalak, Zizka, & Weising, 2020). Bromeliaceae as a whole is considered an adaptive radiation (Benzing, 2000;Givnish et al, 2011) and contains several rapidly radiating lineages, most notably within Bromelioideae (Aguirre-Santoro, Salinas, & Michelangeli, 2020) and Tillandsioideae (Loiseau et al, 2021).…”