skip to main content

Title: Signals of differential introgression in the genome of natural hybrids of Caribbean anoles

Hybridization facilitates recombination between divergent genetic lineages and can be shaped by both neutral and selective processes. Upon hybridization, loci with no net fitness effects introgress randomly from parental species into the genomes of hybrid individuals. Conversely, alleles from one parental species at some loci may provide a selective advantage to hybrids, resulting in patterns of introgression that do not conform to random expectations. We investigated genomic patterns of differential introgression in natural hybrids of two species of Caribbean anoles,Anolis pulchellusandA. krugiin Puerto Rico. Hybrids exhibitA. pulchellusphenotypes but possessA. krugimitochondrial DNA, originated from multiple, independent hybridization events, and appear to have replaced pureA. pulchellusacross a large area in western Puerto Rico. Combining genome‐wide SNP datasets with bioinformatic methods to identify signals of differential introgression in hybrids, we demonstrate that the genomes of hybrids are dominated bypulchellus‐derived alleles and show only 10%–20%A. krugiancestry. The majority ofA. krugiloci in hybrids exhibit a signal of non‐random differential introgression and include loci linked to genes involved in development and immune function. Three of these genes (delta like canonical notch ligand 1, jagged1 and notch receptor 1) affect cell differentiation and growth and interact with mitochondrial function. Our results suggest that differential non‐random introgression for a subset of loci may be driven by selection favouring the inheritance of compatible mitochondrial and nuclear‐encoded genes in hybrids.

more » « less
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Date Published:
Journal Name:
Molecular Ecology
Medium: X Size: p. 6000-6017
["p. 6000-6017"]
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Invasive species can impact native populations through competition, predation, habitat alteration, and disease transmission, but also genetically through hybridization. Potential outcomes of hybridization span the continuum from extinction to hybrid speciation and can be further complicated by anthropogenic habitat disturbance. Hybridization between the native green anole lizard (Anolis carolinensis) and a morphologically similar invader (A. porcatus) in south Florida provides an ideal opportunity to study interspecific admixture across a heterogeneous landscape. We used reduced‐representation sequencing to describe introgression in this hybrid system and to test for a relationship between urbanization and non‐native ancestry. Our findings indicate that hybridization between green anole lineages was probably a limited, historic event, producing a hybrid population characterized by a diverse continuum of ancestry proportions. Genomic cline analyses revealed rapid introgression and disproportionate representation of non‐native alleles at many loci and no evidence for reproductive isolation between parental species. Three loci were associated with urban habitat characteristics; urbanization and non‐native ancestry were positively correlated, although this relationship did not remain significant when accounting for spatial nonindependence. Ultimately, our study demonstrates the persistence of non‐native genetic material even in the absence of ongoing immigration, indicating that selection favouring non‐native alleles can override the demographic limitation of low propagule pressure. We also note that not all outcomes of admixture between native and non‐native species should be considered intrinsically negative. Hybridization with ecologically robust invaders can lead to adaptive introgression, which may facilitate the long‐term survival of native populations otherwise unable to adapt to anthropogenically mediated global change.

    more » « less
  2. Abstract

    Polymorphisms for melanic form of insects may provide various selective advantages. However, melanic alleles may have significant/subtle pleiotrophic “costs.” Several potential pleiotrophic effects of the W (=Y)‐linked melanism gene inPapilio glaucusL. (Lepidoptera) showed no costs for melanic versus yellow in adult size, oviposition preferences, fecundity, egg viability, larval survival/growth rates, cold stress tolerance, or postdiapause emergence times. Sexual selection (males choosing yellow rather than mimetic dark females) had been suggested to provide a balanced polymorphism inP. glaucus, but spermatophore counts in wild females and direct field tethering studies of size‐matched pairs of virgin females (dark and yellow), show that male preferences are random or frequency‐dependent from Florida to Michigan, providing no yellow counter‐advantages. Recent frequency declines of dark (melanic/mimetic) females inP. glaucuspopulations are shown in several major populations from Florida (27.3°N latitude) to Ohio (38.5° N). Summer temperatures have increased significantly at all these locations during this time (1999–2018), but whether dark morphs may be more vulnerable (in any stage) to such climate warming remains to be determined. Additional potential reasons for the frequency declines in mimetic females are discussed: (i) genetic introgression of Z‐linked melanism suppressor genes fromP. canadensis(R & J) and the hybrid species,P. appalachiensis(Pavulaan & Wright), (ii) differential developmental incompatibilities, or Haldane effects, known to occur in hybrids, (iii) selection against intermediately melanic (“dusty”) females (with the W‐linked melanic gene, b+) which higher temperatures can cause.

    more » « less
  3. Abstract

    Understanding how organisms adapt to changing environments is a core focus of research in evolutionary biology. One common mechanism is adaptive introgression, which has received increasing attention as a potential route to rapid adaptation in populations struggling in the face of ecological change, particularly global climate change. However, hybridization can also result in deleterious genetic interactions that may limit the benefits of adaptive introgression. Here, we used a combination of genome‐wide quantitative trait locus mapping and differential gene expression analyses between the swordtail fish speciesXiphophorus malincheandX.birchmannito study the consequences of hybridization on thermotolerance. While these two species are adapted to different thermal environments, we document a complicated architecture of thermotolerance in hybrids. We identify a region of the genome that contributes to reduced thermotolerance in individuals heterozygous forX.malincheandX.birchmanniancestry, as well as widespread misexpression in hybrids of genes that respond to thermal stress in the parental species, particularly in the circadian clock pathway. We also show that a previously mapped hybrid incompatibility betweenX.malincheandX.birchmannicontributes to reduced thermotolerance in hybrids. Together, our results highlight the challenges of understanding the impact of hybridization on complex ecological traits and its potential impact on adaptive introgression.

    more » « less
  4. Abstract

    Despite the presence of reproductive barriers between species, interspecific gene introgression has been documented in a range of natural systems. Comparing patterns of genetic introgression in biparental versus matrilineal markers can potentially reveal sex‐specific barriers to interspecific gene flow. Hybridization has been documented in the freshwater turtlesGraptemys geographicaandG. pseudogeographica, whose ranges are largely sympatric. Morphological differentiation between the species is restricted to females, with femaleG. geographicapossessing large heads and jaws compared to the narrow heads ofG. pseudogeographicafemales. If hybrid females are morphologically intermediate, they may be less successful at exploiting parental feeding niches, thereby limiting the introgression of maternally inherited, but not biparental, molecular markers. We paired sequence data with stable isotope analysis and examined sex‐specific genetic introgression and trophic differentiation in sympatric populations ofG. geographicaandG. pseudogeographica. We observed introgression fromG. pseudogeographicaintoG. geographicaat three nuclear loci, but not at the mitochondrial locus. Analysis of ∂15N and ∂13C was consistent with species differences in trophic positioning in females, but not males. These results suggest that ecological divergence in females may reduce the opportunity for gene flow in this system.

    more » « less
  5. 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