Genome Skimming Reveals Widespread Hybridization in a Neotropical Flowering Plant Radiation

Abstract

The tropics hold at least an order of magnitude greater plant diversity than the temperate zone, yet the reasons for this difference are still subject to debate. Much of tropical plant diversity is in highly speciose genera and understanding the drivers of such high species richness will help solve the tropical diversity enigma. Hybridization has recently been shown to underlie many adaptive radiations, but its role in the evolution of speciose tropical plant genera has received little attention. Here, we address this topic in the hyperdiverse Bromeliaceae genus Vriesea using genome skimming data covering the three genomic compartments. We find evidence for hybridization in ca. 11% of the species in our dataset, both within the genus and between Vriesea and other genera, which is commensurate with hybridization underlying the hyperdiversity of Vriesea, and potentially other genera in Tillandsioideae. While additional genomic research will be needed to further clarify the contribution of hybridization to the rapid diversification of Vriesea, our study provides an important first data point suggesting its importance to the evolution of tropical plant diversity.

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

“…Beyond the scope of this study, the availability of a bait set kit for Bromeliaceae provides a prime genetic resource for investigating several topical research questions on the origin and maintenance of Bromeliaceae diversity. Manyfold studies of bromeliad phylogenomics set force the challenges of resolving species-level phylogenies with a small number of markers, particularly in young and speciose groups (Goetze, Zanella, Palma-Silva, Büttow, & Bered, 2017; Granados Mendoza et al, 2017; Loiseau et al, 2021; Versieux et al, 2012). This particularly curated bait set allows highly efficient sequencing across taxa: within our study, we found high mapping success with 82.3% average read mapping.…”

“…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).…”

“…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). It is a species-rich and charismatic monocot family, consisting of over 3,000 species, including crops in the genus Ananas and other economically important species (Luther, 2008).…”

Speciation with gene flow between two Neotropical sympatric species (Pitcairnia spp.: Bromeliaceae)

“…While it can result in reduction or loss of differentiation in some cases (e.g., Balao et al, 2015 ; Lepais et al, 2009 ), hybridization may represent an important source of adaptive genetic variation through introgression of selectively favored alleles from one population into another. Interspecific gene flow may increase the genetic diversity of introgressed taxa and contribute to speciation process and may act as a source of variation for rapid adaptive radiations (Abbott et al, 2013 ; Gardner & Vose, 2005 ; Lexer et al, 2016 ; Loiseau et al, 2021 ; Mallet, 2007 ; Palma‐Silva et al, 2016 ; Runemark et al, 2019 ; Seehausen, 2004 ). In this context, Bromeliaceae family is one of the best characterized and studied example of adaptive radiation in Neotropics (Barbará et al, 2008 ; Givnish et al, 2011 , 2014 , 2015 ; Palma‐Silva, Leal, et al, 2016 ).…”

“…In this context, Bromeliaceae family is one of the best characterized and studied example of adaptive radiation in Neotropics (Barbará et al, 2008 ; Givnish et al, 2011 , 2014 , 2015 ; Palma‐Silva, Leal, et al, 2016 ). Interspecific gene flow has been largely reported in this plant family (Gardner, 1984 ; Goetze et al, 2017 ; Gonçalves & de Azevêdo‐Gonçalves, 2009 ; Mota et al, 2019 ; Mota et al, 2020 ; Neri et al, 2017 ; Palma‐Silva et al, 2011 ; Palma‐Silva et al, 2015 ; Schulte et al, 2010 ; Wendt et al, 2001 ; Zanella et al, 2016 ) and both ancient and contemporary hybridization are considered to be important to the diversification of this Neotropical radiation (i.e., Goetze et al, 2017 ; Loiseau et al, 2021 ; Neri et al, 2017 ; Mota et al, 2019 ; Mota et al, 2020 , and see review of Palma‐Silva, Leal, et al, 2016 ). A growing body of studies based on molecular markers evaluating hybridization and interspecific gene flow between species of Bromeliaceae have shown that, despite hybridization, the interplay between pre‐ and postzygotic reproductive isolation barriers is important in maintaining species integrity (e.g., Lexer et al, 2016 ; Matallana et al, 2010 ; Mota et al, 2019 , 2020 ; Neri et al, 2017 ; Palma‐Silva et al, 2011 , 2015 ; Schulte et al, 2010 ; Souza et al, 2017 ; Wagner et al, 2015 ; Zanella et al, 2016 ).…”