Ancient and recent introgression shape the evolutionary history of pollinator adaptation and speciation in a model monkeyflower radiation (MimulussectionErythranthe)

Abstract

Inferences about past processes of adaptation and speciation require a gene-scale and genome-wide understanding of the evolutionary history of diverging taxa. In this study, we use genome-wide capture of nuclear gene sequences, plus skimming of organellar sequences, to investigate the phylogenomics of monkeyflowers in Mimulus section Erythranthe (27 accessions from seven species). Taxa within Erythranthe, particularly the parapatric and putatively sister species M. lewisii (bee-pollinated) and M. cardinalis (hummingbird-pollinated), have been a model system for investigating the ecological genetics of speciation and adaptation for over five decades. Across >8000 nuclear loci, multiple methods resolve a predominant species tree in which M. cardinalis groups with other hummingbird-pollinated taxa (37% of gene trees), rather than being sister to M. lewisii (32% of gene trees). We independently corroborate a single evolution of hummingbird pollination syndrome in Erythranthe by demonstrating functional redundancy in genetic complementation tests of floral traits in hybrids; together, these analyses overturn a textbook case of pollination-syndrome convergence. Strong asymmetries in allele-sharing (Patterson’s D-statistic and related tests) indicate that gene-tree discordance reflects ancient and recent introgression rather than incomplete lineage sorting. Consistent with abundant introgression blurring the history of divergence, low-recombination and adaptation-associated regions support the new species tree, while high-recombination regions generate phylogenetic evidence for sister status for M. lewisii and M. cardinalis. Population-level sampling of core taxa also revealed two instances of chloroplast capture, with Sierran M. lewisii and Southern Californian M. parishii each carrying organelle genomes nested within respective sympatric M. cardinalis clades. A recent organellar transfer from M. cardinalis, an outcrosser where selfish cytonuclear dynamics are more likely, may account for the unexpected cytoplasmic male sterility effects of selfer M. parishii organelles in hybrids with M. lewisii. Overall, our phylogenomic results reveal extensive reticulation throughout the evolutionary history of a classic monkeyflower radiation, suggesting that natural selection (re-)assembles and maintains species-diagnostic traits and barriers in the face of gene flow. Our findings further underline the challenges, even in reproductively isolated species, in distinguishing re-use of adaptive alleles from true convergence and emphasize the value of a phylogenomic framework for reconstructing the evolutionary genetics of adaptation and speciation.Author SummaryAdaptive radiations, which involve both divergent evolution of new traits and recurrent trait evolution, provide insight into the processes that generate and maintain organismal diversity. However, rapid radiations also generate particular challenges for inferring the evolutionary history and mechanistic basis of adaptation and speciation, as multiple processes can cause different parts of the genome to have distinct phylogenetic trees. Thus, inferences about the mode and timing of divergence and the causes of parallel trait evolution require a fine-grained understanding of the flow of genomic variation through time. In this study, we used genome-wide sampling of thousands of genes to re-construct the evolutionary histories of a model plant radiation, the monkeyflowers of Mimulus section Erythranthe. Work over the past half-century has established the parapatric and putatively sister species M. lewisii (bee-pollinated) and M. cardinalis (hummingbird-pollinated, as are three other species in the section) as textbook examples of both rapid speciation via shifts in pollination syndrome and convergent evolution of floral syndromes. Our phylogenomic analyses re-write both of these stories, placing M. cardinalis in a clade with other hummingbird-pollinated taxa and demonstrating that abundant introgression between ancestral lineages as well as in areas of current sympatry contributes to the real (but misleading) affinities between M. cardinalis and M. lewisii. This work illustrates the pervasive influence of gene flow and introgression during adaptive radiation and speciation, and underlines the necessity of a gene-scale and genome-wide phylogenomics framework for understanding trait divergence, even among well-established species.

Selective sorting of ancestral introgression in maize and teosinte along an elevational cline

“…When there is widespread selection against introgressing variants at many loci across the genome, selection will more efficiently remove linked ancestry in regions of the genome with lower recombination rates, which creates a positive relationship between local recombination rate and the proportion of introgressed ancestry [1,10,26,39,45,46,59,65,87,89,102]. To test whether such negative selection is shaping patterns of introgression genomewide in sympatric maize and mexicana , we first divided the genome into quintiles based on the local recombination rates for 1 cM windows.…”

“…due to hybrid incompatibilities [76,77,115]. Consistent with the view that hybridization is often deleterious, a growing number of species show evidence of pervasive selection against introgressed ancestry [1,10,26,39,45,46,59,65,87,89]. At the same time, introgression can be a source of novel genetic variation and efficiently introduce haplotypes carrying sets of locally-adapted alleles, with the potential for rapid adaptation to new ecological challenges [71].…”

Comparative analysis of corolla tube development across three closely related Mimulus species with different pollination syndromes

“…We focus on the developmental bases of corolla tube variation in the Mimulus lewisii species complex, which contains several closely related species with striking variation in flower size, shape, and color that is related to their pollination strategy (Beardsley et al, 2003; Hiesey et al, 1971; Nelson et al, 2020; Schemske & Bradshaw, 1999; Vickery & Wullstein, 1987; Yuan, 2019). For example, M. lewisii is an outcrossing, bee‐pollinated species and has flowers with long corolla tubes and flared limbs, Mimulus verbenaceus is pollinated by hummingbirds and has flowers with long, narrow tubes with less flare of the limb than M. lewisii .…”

Highly replicated evolution of parapatric ecotypes

“…For instance, a recent phylogenomic analysis of Mimulus section Erythranthe overturned a classical example of putative convergence in hummingbird pollination (Beardsley et al 2004;Freeman and Herron 2004). The authors discovered that hummingbird pollination in the genus arose only once, yet over a large portion of the genome, sympatric populations of M. cardinalis (hummingbird-pollinated) and M. lewisii (bee-pollinated) appear as sister taxa in the phylogeny because of multiple introgression events after periods of allopatry (Nelson et al 2021). To understand how demography, geography and selection contribute to our interpretations of parallel evolution, first consider a scenario where an ancestral population gives rise to two locally adapted populations that occupy ecologically distinct yet geographically proximate habitats (hereafter ecotypes, Fig.…”