Pleistocene glacial cycles drive isolation, gene flow and speciation in the high‐elevation Andes

Abstract

Mountain ranges are amongst the most species-rich habitats, with many large and rapid evolutionary radiations. The tempo and mode of diversification in these systems are key unanswered questions in evolutionary biology. Here we study the Andean Lupinus radiation to understand the processes driving very rapid diversification in montane systems. We use genomic and transcriptomic data of multiple species and populations, and apply phylogenomic and demographic analyses to test whether diversification proceeded without interspecific gene flow - as expected if Andean orogeny and geographic isolation were the main drivers of diversification - or if diversification was accompanied by gene flow, in which case other processes were probably involved. We uncover several episodes of gene flow between species, including very recent events likely to have been prompted by changes in habitat connectivity during Pleistocene glacial cycles. Furthermore, we find that gene flow between species was heterogeneously distributed across the genome. We argue that exceptionally fast diversification of Andean Lupinus was partly a result of Late Pleistocene glacial cycles, with associated cycles of expansion and contraction driving geographic isolation or secondary contact of species. Furthermore, heterogeneous gene flow across the genome suggests a role for selection and ecological speciation in rapid diversification in this system.

Geological and climatic influences on mountain biodiversity

“…In the relatively young northern Andes, high diversity may be related to surface uplift 27 , which allowed the establishment and subsequent local diversification of cool-adapted lineages of animals 28 and plants 29,30 , although a connection between diversification and orogeny is not always evident 31 . This area is also characterised by many recent species radiations, commonly linked to the influence of glacial-interglacial cycles 32,33,34,35 . In the older central Andes, the orographic barrier is particularly strong, with a warm, wet northeastern side supporting high diversity, and a colder and drier southwestern side with low diversity.…”

Strong divergent selection at multiple loci in two closely related species of ragworts adapted to high and low elevations on Mount Etna

“…SFS of the species pair was first analysed under 14 models of isolation with migration and secondary contact ( Figure S2), which were published previously Nevado, Contreras-Ortiz, Hughes, & Filatov, 2018;Tine et al, 2014) or modified from them. SFS of the species pair was first analysed under 14 models of isolation with migration and secondary contact ( Figure S2), which were published previously Nevado, Contreras-Ortiz, Hughes, & Filatov, 2018;Tine et al, 2014) or modified from them.…”

“…Following recommendations in the dadi manual, each group's sample size was projected down to 10-14 alleles (i.e., SNPs with less than these numbers of alleles scored will be removed, and those with more were subsampled to these numbers) to deal with missing data across individuals. SFS of the species pair was first analysed under 14 models of isolation with migration and secondary contact ( Figure S2), which were published previously Nevado, Contreras-Ortiz, Hughes, & Filatov, 2018;Tine et al, 2014) or modified from them. These models vary in complexity (see detailed flow chart in Figure S2), with the simplest one (split) having no population size change and no migration between populations since splitting; to more complex models that allow migration rate in one direction only (e.g., IM1, IM2), same migration rate for both directions (e.g., split_mig, IM2M_1), different migration rates in each direction (e.g., SC, IM, IMpre), different migration rates at different times (e.g., SplitExpMig, eSplitExpMig) or at different parts of genome (e.g.…”

Advances in legume research in the genomics era

“…Next-generation sequencing data provide more than just phylogenetic resolution and their application to elucidating adaptive radiations and diversification is just beginning. This is exemplified in ground-breaking studies on Lupinus, a genus of 280 species, with a series of nested and parallel rapid radiations in North and South America (Hughes and Eastwood 2006) where the genus exhibits startling diversity in growth form and habitat in the Andes, a radiation that is likely to have been spurred by Pleistocene glacial cycles (Nevado et al 2018). Furthermore, lineage-specific diversification rates were detected across the phylogeny, but the ability to ascertain the processes underpinning rapid species radiations remained elusive.…”