skip to main content


Title: Biased gene retention in the face of introgression obscures species relationships
Abstract Phylogenomic analyses are recovering previously hidden histories of hybridization, revealing the genomic consequences of these events on the architecture of extant genomes. We applied phylogenomic techniques and several complementary statistical tests to show that introgressive hybridization appears to have occurred between close relatives of Arabidopsis, resulting in cytonuclear discordance and impacting our understanding of species relationships in the group. The composition of introgressed and retained genes indicates that selection against incompatible cytonuclear and nuclear-nuclear interactions likely acted during introgression, while linkage also contributed to genome composition through the retention of ancient haplotype blocks. We also applied divergence-based tests to determine the species branching order and distinguish donor from recipient lineages. Surprisingly, these analyses suggest that cytonuclear discordance arose via extensive nuclear, rather than cytoplasmic, introgression. If true, this would mean that most of the nuclear genome was displaced during introgression, while only a small proportion of native alleles were retained.  more » « less
Award ID(s):
2021753
NSF-PAR ID:
10182300
Author(s) / Creator(s):
; ;
Date Published:
Journal Name:
Genome Biology and Evolution
ISSN:
1759-6653
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Buerkle, Alex (Ed.)
    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. 
    more » « less
  2. Kubatko, Laura (Ed.)
    Abstract Evidence from natural systems suggests that hybridization between animal species is more common than traditionally thought, but the overall contribution of introgression to standing genetic variation within species remains unclear for most animal systems. Here, we use targeted exon capture to sequence thousands of nuclear loci and complete mitochondrial genomes from closely related chipmunk species in the Tamias quadrivittatus group that are distributed across the Great Basin and the central and southern Rocky Mountains of North America. This recent radiation includes six overlapping, ecologically distinct species (Tamias canipes, Tamias cinereicollis, Tamias dorsalis, T. quadrivittatus, Tamias rufus, and Tamias umbrinus) that show evidence for widespread introgression across species boundaries. Such evidence has historically been derived from a handful of markers, typically focused on mitochondrial loci, to describe patterns of introgression; consequently, the extent of introgression of nuclear genes is less well characterized. We conducted a series of phylogenomic and species-tree analyses to resolve the phylogeny of six species in this group. In addition, we performed several population-genomic analyses to characterize nuclear genomes and infer coancestry among individuals. Furthermore, we used emerging quartets-based approaches to simultaneously infer the species tree (SVDquartets) and identify introgression (HyDe). We found that, in spite of rampant introgression of mitochondrial genomes between some species pairs (and sometimes involving up to three species), there appears to be little to no evidence for nuclear introgression. These findings mirror other genomic results where complete mitochondrial capture has occurred between chipmunk species in the absence of appreciable nuclear gene flow. The underlying causes of recurrent massive cytonuclear discordance remain unresolved in this group but mitochondrial DNA appears highly misleading of population histories as a whole. Collectively, it appears that chipmunk species boundaries are largely impermeable to nuclear gene flow and that hybridization, while pervasive with respect to mtDNA, has likely played a relatively minor role in the evolutionary history of this group. [Cytonuclear discordance; hyridization; introgression, phylogenomics; SVDquartets; Tamias.] 
    more » « less
  3. Abstract

    Gametic isolation is thought to play an important role in the evolution of reproductive isolation in broadcast‐spawning marine invertebrates. However, it is unclear whether gametic isolation commonly evolves early in the speciation process or only accumulates after other reproductive barriers are already in place. It is also unknown whether gametic isolation is an effective barrier to introgression following speciation. Here, we used whole‐genome sequencing data and multiple complementary phylogenomic approaches to test whether the well‐documented gametic incompatibilities among the strongylocentrotid sea urchins have limited introgression. We quantified phylogenetic discordance, inferred reticulate phylogenetic networks, and applied theΔstatistic using gene tree topologies reconstructed from multiple sequence alignments of protein‐coding single‐copy orthologs. In addition, we conducted ABBA–BABA tests on genome‐wide single nucleotide variants and reconstructed a phylogeny of mitochondrial genomes. Our results revealed strong mito‐nuclear discordance and considerable nonrandom gene tree discordance that cannot be explained by incomplete lineage sorting alone. Eight of the nine species examined demonstrated a history of introgression with at least one other species or ancestral lineage, indicating that introgression was common during the diversification of the strongylocentrotid urchins. There was strong support for introgression between four extant species pairs (Strongylocentrotus pallidusS. droebachiensis,S. intermediusS. pallidus,S. purpuratusS. fragilis, andMesocentrotus franciscanusPseudocentrotus depressus) and additional evidence for introgression on internal branches of the phylogeny. Our results suggest that the existing gametic incompatibilities among the strongylocentrotid urchin species have not been a complete barrier to hybridization and introgression following speciation. Their continued divergence in the face of widespread introgression indicates that other reproductive isolating barriers likely exist and may have been more critical in establishing reproductive isolation early in speciation.

     
    more » « less
  4. Introgression can produce novel genetic variation in organisms that hybridize. Sympatric species pairs in the carnivorous plant genusSarraceniaL. frequently hybridize, and all known hybrids are fertile. Despite being a desirable system for studying the evolutionary consequences of hybridization, the extent to which introgression occurs in the genus is limited to a few species in only two field sites. Previous phylogenomic analysis ofSarraceniaestimated a highly resolved species tree from 199 nuclear genes, but revealed a plastid genome that is highly discordant with the species tree. Such cytonuclear discordance could be caused by chloroplast introgression (i.e. chloroplast capture) or incomplete lineage sorting (ILS). To better understand the extent to which introgression is occurring inSarracenia, the chloroplast capture and ILS hypotheses were formally evaluated. Plastomes were assembledde-novofrom sequencing reads generated from 17 individuals in addition to reads obtained from the previous study. Assemblies of 14 whole plastomes were generated and annotated, and the remaining fragmented assemblies were scaffolded to these whole-plastome assemblies. Coding sequence from 79 homologous genes were aligned and concatenated for maximum-likelihood phylogeny estimation. The plastome tree is extremely discordant with the published species tree. Plastome trees were simulated under the coalescent and tree distance from the species tree was calculated to generate a null distribution of discordance that is expected under ILS alone. A t-test rejected the null hypothesis that ILS could cause the level of discordance seen in the plastome tree, suggesting that chloroplast capture must be invoked to explain the discordance. Due to the extreme level of discordance in the plastome tree, it is likely that chloroplast capture has been common in the evolutionary history ofSarracenia.

     
    more » « less
  5. Abstract

    Hybridization, introgression, and reciprocal gene flow during speciation, specifically the generation of mitonuclear discordance, are increasingly observed as parts of the speciation process. Genomic approaches provide insight into where, when, and how adaptation operates during and after speciation and can measure historical and modern introgression. Whether adaptive or neutral in origin, hybridization can cause mitonuclear discordance by placing the mitochondrial genome of one species (or population) in the nuclear background of another species. The latter, introgressed species may eventually have its own mtDNA replaced or “captured” by other species across its entire geographical range. Intermediate stages in the capture process should be observable. Two nonsister species of Australasian monarch‐flycatchers, Spectacled Monarch (Symposiachrus trivirgatus) mostly of Australia and Indonesia and Spot‐winged Monarch (S. guttula) of New Guinea, present an opportunity to observe this process. We analysed thousands of single nucleotide polymorphisms (SNPs) derived from ultraconserved elements of all subspecies of both species. Mitochondrial DNA sequences of Australian populations ofS. trivirgatusform two paraphyletic clades, one being sister to and presumably introgressed byS. guttuladespite little nuclear signal of introgression. Population genetic analyses (e.g., tests for modern and historical gene flow and selection) support at least one historical gene flow event betweenS. guttulaand AustralianS. trivirgatus. We also uncovered introgression from the Maluku Islands subspecies ofS. trivirgatusinto an island population ofS. guttula, resulting in apparent nuclear paraphyly. We find that neutral demographic processes, not adaptive introgression, are the most likely cause of these complex population histories. We suggest that a Pleistocene extinction ofS. guttulafrom mainland Australia resulted from range expansion byS. trivirgatus.

     
    more » « less