skip to main content

Title: Ancient and recent introgression shape the evolutionary history of pollinator adaptation and speciation in a model monkeyflower radiation (Mimulus section Erythranthe)
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 more » 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. « less
; ; ; ; ;
Buerkle, Alex
Award ID(s):
Publication Date:
Journal Name:
PLOS Genetics
Page Range or eLocation-ID:
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Phylogenomic data from a rapidly increasing number of studies provide new evidence for resolving relationships in recently radiated clades, but they also pose new challenges for inferring evolutionary histories. Most existing methods for reconstructing phylogenetic hypotheses rely solely on algorithms that only consider incomplete lineage sorting (ILS) as a cause of intra- or intergenomic discordance. Here, we utilize a variety of methods, including those to infer phylogenetic networks, to account for both ILS and introgression as a cause for nuclear and cytoplasmic-nuclear discordance using phylogenomic data from the recently radiated flowering plant genus Polemonium (Polemoniaceae), an ecologically diverse genus in Western North America with known and suspected gene flow between species. We find evidence for widespread discordance among nuclear loci that can be explained by both ILS and reticulate evolution in the evolutionary history of Polemonium. Furthermore, the histories of organellar genomes show strong discordance with the inferred species tree from the nuclear genome. Discordance between the nuclear and plastid genome is not completely explained by ILS, and only one case of discordance is explained by detected introgression events. Our results suggest that multiple processes have been involved in the evolutionary history of Polemonium and that the plastid genomemore »does not accurately reflect species relationships. We discuss several potential causes for this cytoplasmic-nuclear discordance, which emerging evidence suggests is more widespread across the Tree of Life than previously thought. [Cyto-nuclear discordance, genomic discordance, phylogenetic networks, plastid capture, Polemoniaceae, Polemonium, reticulations.]« less
  2. Floral divergence can contribute to reproductive isolation among plant lineages, and thus provides an opportunity to study the genetics of speciation, including the number, effect size, mode of action and interactions of quantitative trait loci (QTL). Moreover, flowers represent suites of functionally interrelated traits, but it is unclear to what extent the phenotypic integration of the flower is underlain by a shared genetic architecture, which could facilitate or constrain correlated evolution of floral traits. Here, we examine the genetic architecture of floral morphological traits involved in an evolutionary switch from bill to forehead pollen placement between two species of hummingbird-pollinated Neotropical understorey herbs that are reproductively isolated by these floral differences. For the majority of traits, we find multiple QTL of relatively small effect spread throughout the genome. We also find substantial colocalization and alignment of effects of QTL underlying different floral traits that function together to promote outcrossing and reduce heterospecific pollen transfer. Our results are consistent with adaptive pleiotropy or linkage of many co-adapted genes, either of which could have facilitated a response to correlated selection and helped to stabilize divergent phenotypes in the face of low levels of hybridization. Moreover, our results indicate that floral mechanical isolationmore »can be consistent with an infinitesimal model of adaptation.« less
  3. Abstract

    Baobabs (Adansonia) are a cohesive group of tropical trees with a disjunct distribution in Australia, Madagascar, and continental Africa, and diverse flowers associated with two pollination modes. We used custom-targeted sequence capture in conjunction with new and existing phylogenetic comparative methods to explore the evolution of floral traits and pollination systems while allowing for reticulate evolution. Our analyses suggest that relationships in Adansonia are confounded by reticulation, with network inference methods supporting at least one reticulation event. The best supported hypothesis involves introgression between Adansonia rubrostipa and core Longitubae, both of which are hawkmoth pollinated with yellow/red flowers, but there is also some support for introgression between the African lineage and Malagasy Brevitubae, which are both mammal-pollinated with white flowers. New comparative methods for phylogenetic networks were developed that allow maximum-likelihood inference of ancestral states and were applied to study the apparent homoplasy in floral biology and pollination mode seen in Adansonia. This analysis supports a role for introgressive hybridization in morphological evolution even in a clade with highly divergent and geographically widespread species. Our new comparative methods for discrete traits on species networks are implemented in the software PhyloNetworks. [Comparative methods; Hyb-Seq; introgression; network inference; population trees; reticulatemore »evolution; species tree inference; targeted sequence capture.]

    « less
  4. Smith, Stephen (Ed.)
    Abstract Understanding how gene flow affects population divergence and speciation remains challenging. Differentiating one evolutionary process from another can be difficult because multiple processes can produce similar patterns, and more than one process can occur simultaneously. Although simple population models produce predictable results, how these processes balance in taxa with patchy distributions and complicated natural histories is less certain. These types of populations might be highly connected through migration (gene flow), but can experience stronger effects of genetic drift and inbreeding, or localized selection. Although different signals can be difficult to separate, the application of high-throughput sequence data can provide the resolution necessary to distinguish many of these processes. We present whole-genome sequence data for an avian species group with an alpine and arctic tundra distribution to examine the role that different population genetic processes have played in their evolutionary history. Rosy-finches inhabit high elevation mountaintop sky islands and high-latitude island and continental tundra. They exhibit extensive plumage variation coupled with low levels of genetic variation. Additionally, the number of species within the complex is debated, making them excellent for studying the forces involved in the process of diversification, as well as an important species group in which to investigatemore »species boundaries. Total genomic variation suggests a broadly continuous pattern of allele frequency changes across the mainland taxa of this group in North America. However, phylogenomic analyses recover multiple distinct, well supported, groups that coincide with previously described morphological variation and current species-level taxonomy. Tests of introgression using D-statistics and approximate Bayesian computation reveal significant levels of introgression between multiple North American taxa. These results provide insight into the balance between divergent and homogenizing population genetic processes and highlight remaining challenges in interpreting conflict between different types of analytical approaches with whole-genome sequence data. [ABBA-BABA; approximate Bayesian computation; gene flow; phylogenomics; speciation; whole-genome sequencing.]« less
  5. Green plants (Viridiplantae) include around 450,000–500,000 species of great diversity and have important roles in terrestrial and aquatic ecosystems. Here, as part of the One Thousand Plant Transcriptomes Initiative, we sequenced the vegetative transcriptomes of 1,124 species that span the diversity of plants in a broad sense (Archaeplastida), including green plants (Viridiplantae), glaucophytes (Glaucophyta) and red algae (Rhodophyta). Our analysis provides a robust phylogenomic framework for examining the evolution of green plants. Most inferred species relationships are well supported across multiple species tree and supermatrix analyses, but discordance among plastid and nuclear gene trees at a few important nodes highlights the complexity of plant genome evolution, including polyploidy, periods of rapid speciation, and extinction. Incomplete sorting of ancestral variation, polyploidization and massive expansions of gene families punctuate the evolutionary history of green plants. Notably, we find that large expansions of gene families preceded the origins of green plants, land plants and vascular plants, whereas whole-genome duplications are inferred to have occurred repeatedly throughout the evolution of flowering plants and ferns. The increasing availability of high-quality plant genome sequences and advances in functional genomics are enabling research on genome evolution across the green tree of life.