Ancient hybridization leads to the repeated evolution of red flowers across a monkeyflower radiation

Abstract

The reuse of old genetic variation can promote rapid diversification in evolutionary radiations, but in most cases, the historical events underlying this divergence are not known. For example, ancient hybridization can generate new combinations of alleles that sort into descendant lineages, potentially providing the raw material to initiate divergence. In the Mimulus aurantiacus species complex, there is evidence for widespread gene flow among members of this radiation. In addition, allelic variation in the MaMyb2 gene is responsible for differences in flower color between the closely related ecotypes of subspecies puniceus, contributing to reproductive isolation by pollinators. Previous work suggested that MaMyb2 was introgressed into the red-flowered ecotype of puniceus. However, additional taxa within the radiation have independently evolved red flowers from their yellow-flowered ancestors, raising the possibility that this introgression had a more ancient origin. In this study, we used repeated tests of admixture from whole-genome sequence data across this diverse radiation to demonstrate that there has been both ancient and recurrent hybridization in this group. However, most of the signal of this ancient introgression has been removed due to selection, suggesting that widespread barriers to gene flow are in place between taxa. Yet, a roughly 30 kb region that contains the MaMyb2 gene is currently shared only among the red-flowered taxa. Patterns of admixture, sequence divergence, and extended haplotype homozygosity across this region confirm a history of ancient hybridization, where functional variants have been preserved due to positive selection in red-flowered taxa but lost in their yellow-flowered counterparts. The results of this study reveal that selection against gene flow can reduce genomic signatures of ancient hybridization, but that historical introgression can provide essential genetic variation that facilitates the repeated evolution of phenotypic traits between lineages.

Complex Hybridization in a Clade of Polytypic Salamanders (Plethodontidae:Desmognathus) Uncovered by Estimating Higher-Level Phylogenetic Networks

“…Mitochondrial data support monophyly of the Nantahala + Pisgah lineages (Kozak et al 2005; Beamer and Lamb 2020), indicating a deep-time reticulation prior to the diversification of the extant lineages (~8-15 Ma; Kozak et al 2005) which has yet to be detected using tree-or SNP-based methods (see Pyron et al 2020). Some similar instances have recently been demonstrated in alpine lake fishes (De-Kayne et al 2022) and monkeyflowers (Short and Streisfeld 2023), where selection has removed much of the signal of ancient introgression that resulted in phenotypic shifts between hybrid lineages through time. Identifying the genetic basis of these black-bellied and shovel-nosed phenotypes, potential subtle differences between the genetic lineages of each, and their phylogenetic origin will be crucial to untangle the complex evolutionary history of the group.…”

“…Here, we find that hybrids are essentially isomorphic with at least one parental lineage (Short and Streisfeld 2023); hybrids are moving back and forth between existing binary fitness peaks. We also see a curious asymmetry in transmission of threshold alleles for the phenotype switch (Fig.…”

“…These repeated contacts may themselves drive evolutionary diversification through hybridization and genetic transfer (Seehausen 2004;Rosenblum et al 2012). The transmission of adaptive alleles and quantitative trait loci via introgression may also induce ecological speciation as hybrids develop novel phenotypes, occupy new adaptive landscapes, or switch between ecomorphs (Hatfield and Schluter 1999;Nolte et al 2005;Rougemont et al 2015;Makowicz and Travis 2020;Short and Streisfeld 2023).…”

“…In simple instances with two parentals and one hybrid, this may be easy to demonstrate (e.g., Gompert et al 2006). Alternatively, the repeated evolution or vertical transmission from standing ancestral variation of alternative ecomorphs may facilitate ecological segregation of parentals and hybrids over repeated instances of introgression (De-Kayne et al 2022;Short and Streisfeld 2023). One might also draw a distinction between ancient, well-established or 'stabilized' hybrid lineages or species and those arising from more recent secondary contact and subsequent admixture (Chaturvedi et al 2020).…”

How the switch to hummingbird pollination has greatly contributed to our understanding of evolutionary processes

“…Moreover, alleles with large effects (whether that be large effects on individual traits or pleiotropic effects on multiple traits) or haplotypes of linked adaptive alleles should introgress more efficiently than polygenic traits specified by many unlinked loci. Our best example of adaptive introgression fueling a switch to hummingbird pollination comes from the Mimulus aurantiacus species complex: A major-effect regulatory mutation to the MaMyb2 gene that confers red flowers has been transferred between lineages through introgression, facilitating repeated switches from yellow to red flowers (Stankowski & Streisfeld, 2015;Short & Streisfeld, 2023). Future phylogenomic studies using whole genome data could reveal whether introgression facilitated repeated shifts to hummingbird pollination in other systems.…”