skip to main content

Title: Deep Ancestral Introgression Shapes Evolutionary History of Dragonflies and Damselflies
Abstract Introgression is an important biological process affecting at least 10% of the extant species in the animal kingdom. Introgression significantly impacts inference of phylogenetic species relationships where a strictly binary tree model cannot adequately explain reticulate net-like species relationships. Here, we use phylogenomic approaches to understand patterns of introgression along the evolutionary history of a unique, nonmodel insect system: dragonflies and damselflies (Odonata). We demonstrate that introgression is a pervasive evolutionary force across various taxonomic levels within Odonata. In particular, we show that the morphologically “intermediate” species of Anisozygoptera (one of the three primary suborders within Odonata besides Zygoptera and Anisoptera), which retain phenotypic characteristics of the other two suborders, experienced high levels of introgression likely coming from zygopteran genomes. Additionally, we find evidence for multiple cases of deep inter-superfamilial ancestral introgression. [Gene flow; Odonata; phylogenomics; reticulate evolution.]  more » « less
Award ID(s):
Author(s) / Creator(s):
; ; ; ; ; ; ; ;
Matschiner, Michael
Date Published:
Journal Name:
Systematic Biology
Page Range / eLocation ID:
526 to 546
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. null (Ed.)
    Introgressive hybridization can be a powerful force impacting patterns of evolution at multiple taxonomic levels. We aimed to understand how introgression has affected speciation and diversification within a species complex of jumping spiders. The Habronattus americanus subgroup is a recently radiating group of jumping spiders, with species now in contact after hypothesized periods of isolation during glaciation cycles of the Pleistocene. Effects of introgression on genomes and morphology were investigated using phylogenomic and clustering methods using RADseq, ultraconserved elements (UCEs), and morphological data. We characterized 14 unique species/morphs using non-metric multidimensional scaling of morphological data, a majority of which were not recovered as monophyletic in our phylogenomic analyses. Morphological clusters and genetic lineages are highly incongruent, such that geographic region was a greater predictor of phylogenetic relatedness and genomic similarity than species or morph identity. STRUCTURE analyses support this pattern, revealing clusters corresponding to larger geographic regions. A history of rapid radiation in combination with frequent introgression seems to have mostly homogenized the genomes of species in this system, while selective forces maintain distinct male morphologies. GEMMA analyses support this idea by identifying SNPs correlated with distinct male morphologies. Overall, we have uncovered a system at odds with a typical bifurcating evolutionary model, instead supporting one where closely related species evolve together connected through multiple introgression events, creating a reticulate evolutionary history. 
    more » « less
  2. 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 genome 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.] 
    more » « less
  3. Abstract

    Abstract.—The origin and eventual loss of biogeographic barriers can create alternating periods of allopatry and secondary contact, facilitating gene flow among distinct metapopulations and generating reticulate evolutionary histories that are not adequately described by a bifurcating evolutionary tree. One such example may exist in the two-lined salamander (Eurycea bislineata) species complex, where discordance among morphological and molecular datasets has created a “vexing taxonomic challenge.” Previous phylogeographic analyses of mitochondrial DNA (mtDNA) suggested that the reorganization of Miocene paleodrainages drove vicariance and dispersal, but the inherent limitations of a single-locus dataset precluded the evaluation of subsequent gene flow. Here, we generate triple-enzyme restriction site-associated DNA sequencing (3RAD) data for > 100 individuals representing all major mtDNA lineages and use a suite of complementary methods to demonstrate that discordance among earlier datasets is best explained by a reticulate evolutionary history influenced by river drainage reorganization. Systematics of such groups should acknowledge these complex histories and relationships that are not strictly hierarchical. [Amphibian; hybridization; introgression; Plethodontidae; stream capture.]

    more » « less
  4. Abstract

    Rodents are the largest order of mammals and contain several model organisms important to scientific research in a variety of fields, yet no large set of genomic markers have been designed for this group to date, hindering evolutionary studies into relationships of the group as a whole. Here we present a genomic probe set designed and optimized for rodents with a protocol that is easy to replicate with little laboratory investment. This design utilizes an anchored hybrid enrichment approach specifically targeting rodents to generate longer loci with a higher substitution rate than existing vertebrate probes to provide utility at various taxonomic levels. Using a test set of rodents from all five suborders, we successfully obtained alignments for 416 of the 418 target loci with an average of 1379 bp per locus and a total alignment of more than half a million base pairs. This genomic data set performed well in all phylogenetic analyses, especially in recent phylogenetic splits, with ample parsimony‐informative sites within genera and even within species, showing more than four times as many single nucleotide polymorphisms per locus than a recent vertebrate ultraconserved elements study. Additional support is provided in resolving deeper clades in Rodentia. By providing this probe design, we hope that more laboratories can easily generate data for answering questions in rodents from species delimitation to understanding relationships among families in rapid radiations.

    more » « less
  5. Abstract

    The role of hybridization and subsequent introgression has been demonstrated in an increasing number of species. Recently, Fontaineet al. (Science, 347, 2015, 1258524) conducted a phylogenomic analysis of six members of theAnopheles gambiaespecies complex. Their analysis revealed a reticulate evolutionary history and pointed to extensive introgression on all four autosomal arms. The study further highlighted the complex evolutionary signals that the co‐occurrence of incomplete lineage sorting (ILS) and introgression can give rise to in phylogenomic analyses. While tree‐based methodologies were used in the study, phylogenetic networks provide a more natural model to capture reticulate evolutionary histories. In this work, we reanalyse theAnophelesdata using a recently devised framework that combines the multispecies coalescent with phylogenetic networks. This framework allows us to captureILSand introgression simultaneously, and forms the basis for statistical methods for inferring reticulate evolutionary histories. The new analysis reveals a phylogenetic network with multiple hybridization events, some of which differ from those reported in the original study. To elucidate the extent and patterns of introgression across the genome, we devise a new method that quantifies the use of reticulation branches in the phylogenetic network by each genomic region. Applying the method to the mosquito data set reveals the evolutionary history of all the chromosomes. This study highlights the utility of ‘network thinking’ and the new insights it can uncover, in particular in phylogenomic analyses of large data sets with extensive gene tree incongruence.

    more » « less