skip to main content


Title: Steep, coincident, and concordant clines in mitochondrial and nuclear‐encoded genes in a hybrid zone between subspecies of Atlantic killifish, Fundulus heteroclitus
Abstract

Steep genetic clines resulting from recent secondary contact between previously isolated taxa can either gradually erode over time or be stabilized by factors such as ecological selection or selection against hybrids. We used patterns of variation in 30 nuclear and two mitochondrialSNPs to examine the factors that could be involved in stabilizing clines across a hybrid zone between two subspecies of the Atlantic killifish,Fundulus heteroclitus. Increased heterozygote deficit and cytonuclear disequilibrium in populations near the center of the mtDNAcline suggest that some form of reproductive isolation such as assortative mating or selection against hybrids may be acting in this hybrid zone. However, only a small number of loci exhibited these signatures, suggesting locus‐specific, rather than genomewide, factors. Fourteen of the 32 loci surveyed had cline widths inconsistent with neutral expectations, with twoSNPs in the mitochondrial genome exhibiting the steepest clines. Seven of the 12 putatively non‐neutral nuclear clines were forSNPs in genes related to oxidative metabolism. Among these putatively non‐neutral nuclear clines,SNPs in two nuclear‐encoded mitochondrial genes (SLC25A3 andHDDC2), as well asSNPs in the myoglobin, 40S ribosomal protein S17, and actin‐bindingLIMprotein genes, had clines that were coincident and concordant with the mitochondrial clines. When hybrid index was calculated using this subset of loci, the frequency distribution of hybrid indices for a population located at the mtDNAcline center was non‐unimodal, suggesting selection against advanced‐generation hybrids, possibly due to effects on processes involved in oxidative metabolism.

 
more » « less
NSF-PAR ID:
10018216
Author(s) / Creator(s):
 ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Ecology and Evolution
Volume:
6
Issue:
16
ISSN:
2045-7758
Format(s):
Medium: X Size: p. 5771-5787
Size(s):
["p. 5771-5787"]
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Introgression might be exceptionally common during the evolution of narrowly endemic species. For instance, in the springs of the small and isolatedCuatroCiénegasValley, the mitogenome of the cichlid fishHerichthys cyanoguttatuscould be rapidly introgressing into populations of the trophically polymorphicH. minckleyi. We used a combination of genetic and environmental data to examine the factors associated with this mitochondrial introgression. A reduced representation library of over 6220 single nucleotide polymorphisms (SNPs) from the nuclear genome showed that mitochondrial introgression intoH. minckleyiis biased relative to the amount of nuclear introgression.SNPassignment probabilities also indicated that cichlids with more hybrid ancestry are not more commonly female providing no support for asymmetric backcrossing or hybrid‐induced sex‐ratio distortion in generating the bias in mitochondrial introgression. Smaller effective population size inH. minckleyiinferred from theSNPs coupled with sequences of all 13 mitochondrial proteins suggests that relaxed selection on the mitogenome could be facilitating the introgression of “H. cyanoguttatus” haplotypes. Additionally, we showed that springs with colder temperatures had greater amounts of mitochondrial introgression fromH. cyanoguttatus. Relaxed selection inH. minckleyicoupled with temperature‐related molecular adaptation could be facilitating mitogenomic introgression intoH. minckleyi.

     
    more » « less
  2. Abstract

    Effective management of threatened and exploited species requires an understanding of both the genetic connectivity among populations and local adaptation. The Olympia oyster (Ostrea lurida), patchily distributed from Baja California to the central coast of Canada, has a long history of population declines due to anthropogenic stressors. For such coastal marine species, population structure could follow a continuous isolation‐by‐distance model, contain regional blocks of genetic similarity separated by barriers to gene flow, or be consistent with a null model of no population structure. To distinguish between these hypotheses inO. lurida, 13,424 single nucleotide polymorphisms (SNPs) were used to characterize rangewide population structure, genetic connectivity, and adaptive divergence. Samples were collected across the species range on the west coast of North America, from southern California to Vancouver Island. A conservative approach for detecting putative loci under selection identified 235SNPs across 129GBSloci, which were functionally annotated and analyzed separately from the remaining neutral loci. While strong population structure was observed on a regional scale in both neutral and outlier markers, neutral markers had greater power to detect fine‐scale structure. Geographic regions of reduced gene flow aligned with known marine biogeographic barriers, such as Cape Mendocino, Monterey Bay, and the currents around Cape Flattery. The outlier loci identified as under putative selection included genes involved in developmental regulation, sensory information processing, energy metabolism, immune response, and muscle contraction. These loci are excellent candidates for future research and may provide targets for genetic monitoring programs. Beyond specific applications for restoration and management of the Olympia oyster, this study lends to the growing body of evidence for both population structure and adaptive differentiation across a range of marine species exhibiting the potential for panmixia. Computational notebooks are available to facilitate reproducibility and future open‐sourced research on the population structure ofO. lurida.

     
    more » « less
  3. Abstract

    Naturally occurring population variation in reproductive mode presents an opportunity for researchers to test hypotheses regarding the evolution of sex. Asexual reproduction frequently assumes a geographical pattern, in which parthenogenesis‐dominated populations are more broadly dispersed than their sexual conspecifics. We evaluate the geographical distribution of genomic signatures associated with parthenogenesis using nuclear and mitochondrialDNAsequence data from two Japanese harvestman sister taxa,Leiobunum manubriatumandLeiobunum globosum. Asexual reproduction is putatively facultative in these species, and female‐biased localities are common in habitat margins. Past karyotypic and current cytometric work indicatesL. globosumis entirely tetraploid, whileL. manubriatummay be either diploid or tetraploid. We estimated species phylogeny, genetic differentiation, diversity, and mitonuclear discordance in females collected across the species range in order to identify range expansion toward marginal habitat, potential for hybrid origin, and persistence of asexual lineages. Our results point to northward expansion of a tetraploid ancestor ofL. manubriatumandL. globosum, coupled with support for greater male gene flow in southernL. manubriatumlocalities. Specimens from localities in the Tohoku and Hokkaido regions were indistinct, particularly those ofL. globosum, potentially due to little mitochondrial differentiation or haplotypic variation. AlthoughL. manubriatumoverlaps withL. globosumacross its entire range,L. globosumwas reconstructed as monophyletic with strong support using mtDNA, and marginal support with nuclear loci. Ultimately, we find evidence for continued sexual reproduction in both species and describe opportunities to clarify the rate and mechanism of parthenogenesis.

     
    more » « less
  4. Abstract

    A major goal of invasion genetics is to determine how establishment histories shape non‐native organisms' genotypes and phenotypes. While domesticated species commonly escape cultivation to invade feral habitats, few studies have examined how this process shapes feral gene pools and traits. We collected genomic and phenotypic data from feral chickens (Gallus gallus) on the Hawaiian island of Kauai to (i) ascertain their origins and (ii) measure standing variation in feral genomes, morphology and behaviour. Mitochondrial phylogenies (D‐loop & whole Mt genome) revealed two divergent clades within our samples. The rare clade also contains sequences from Red Junglefowl (the domestic chicken's progenitor) and ancientDNAsequences from Kauai that predate European contact. This lineage appears to have been dispersed into the east Pacific by ancient Polynesian colonists. The more prevalent MtDNAclade occurs worldwide and includes domesticated breeds developed recently in Europe that are farmed within Hawaii. We hypothesize this lineage originates from recently feralized livestock and found supporting evidence for increasedG. gallusdensity on Kauai within the last few decades.SNPs obtained from whole‐genome sequencing were consistent with historic admixture between Kauai's divergent(G. gallus)lineages. Additionally, analyses of plumage, skin colour and vocalizations revealed that Kauai birds' behaviours and morphologies overlap with those of domestic chickens and Red Junglefowl, suggesting hybrid origins. Together, our data support the hypotheses that (i) Kauai's feralG. gallusdescend from recent invasion(s) of domestic chickens into an ancient Red Junglefowl reservoir and (ii) feral chickens exhibit greater phenotypic diversity than candidate source populations. These findings complicate management objectives for Pacific feral chickens, while highlighting the potential of this and other feral systems for evolutionary studies of invasions.

     
    more » « less
  5. Abstract

    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