skip to main content

Title: Late Pleistocene range expansion of North American topminnows accompanied by admixture and introgression
Abstract Aim

We used genome‐scale sampling to assess the phylogeography of a group of topminnows in theFundulus notatusspecies complex. Two of the species have undergone extensive range expansions resulting in broadly overlapping distributions, and sympatry within drainages has provided opportunities for hybridization and introgression. We assessed the timing and pattern of range expansion in the context of late Pleistocene–Holocene drainage events and evaluated the evidence for introgressive hybridization between species.


Central and southern United States including drainages of the Gulf of Mexico Coastal Plain and portions of the Mississippi River drainage in and around the Central Highlands.


Topminnows, GenusFundulus, subgenusZygonectesFundulus notatus, Fundulus olivaceus, Fundulus euryzonus.


We sampled members of theF. notatusspecies complex throughout their respective ranges, including numerous drainage systems where species co‐occur. We collected genome‐wide single nucleotide polymorphisms (SNPs) using the genotype‐by‐sequencing (GBS) method and subjected data to population genetic analyses to infer the population histories of both species, including explicit tests for admixture and introgression. The methods employed includedSTRUCTURE, principal coordinates analysis, TreeMix and approximate Bayesian computation.


Genetic data are presented for 749 individuals sampled from 14F. notatus, 20F. olivaceusand 2F. euryzonuspopulations. Members of the species complex differed in phylogeographic structure, withF. notatusexhibiting geographic clusters corresponding to Pleistocene coastal drainages andF. olivaceuscomparatively lacking in phylogeographic structure. Evidence for interspecific introgression varied by drainage.

Main conclusions

Populations ofF. notatusandF. olivaceusexhibited contrasting patterns of lineage diversity among coastal drainages, indicating interspecific differences in their Pleistocene southern refugia. Phylogeographic patterns in both species indicated that range expansions into the northern limits of contemporary distributions coincided with and continued subsequent to the Last Glacial Maximum. There was evidence of introgression between species in some, but not all drainages where the species co‐occur, in a pattern that is correlated with previous estimates of hybridization rates.

more » « less
Author(s) / Creator(s):
 ;  ;  
Publisher / Repository:
Date Published:
Journal Name:
Journal of Biogeography
Page Range / eLocation ID:
p. 2126-2140
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    We present a phylogeographic study of at least six reproductively isolated lineages of new world harvester ants within thePogonomyrmex barbatusandP. rugosusspecies group. The genetic and geographic relationships within this clade are complex: Four of the identified lineages show genetic caste determination (GCD) and are divided into two pairs. Each pair has evolved under a mutualistic system that necessitates sympatry. These paired lineages are dependent upon one another because theirGCDrequires interlineage matings for the production of F1 hybrid workers, and intralineage matings are required to produce queens. ThisGCDsystem maintains genetic isolation among these interdependent lineages, while simultaneously requiring co‐expansion and emigration as their distributions have changed over time. It has also been demonstrated that three of these fourGCDlineages have undergone historical hybridization, but the narrower sampling range of previous studies has left questions on the hybrid parentage, breadth, and age of these groups. Thus, reconstructing the phylogenetic and geographic history of this group allows us to evaluate past insights and hypotheses and to plan future inquiries in a more complete historical biogeographic context. Using mitochondrialDNAsequences sampled across most of the morphospecies’ ranges in the U.S.A. and Mexico, we conducted a detailed phylogeographic study. Remarkably, our results indicate that one of theGCDlineage pairs has experienced a dramatic range expansion, despite the genetic load and fitness costs of theGCDsystem. Our analyses also reveal a complex pattern of vicariance and dispersal inPogonomyrmexharvester ants that is largely concordant with models of late Miocene, Pliocene, and Pleistocene range shifts among various arid‐adapted taxa in North America.

    more » « less
  2. Abstract

    Pairs of species that exhibit broadly overlapping distributions, and multiple geographically isolated contact zones, provide opportunities to investigate the mechanisms of reproductive isolation. Such naturally replicated systems have demonstrated that hybridization rates can vary substantially among populations, raising important questions about the genetic basis of reproductive isolation. The topminnows,Fundulus notatusandF. olivaceus, are reciprocally monophyletic, and co‐occur in drainages throughout much of the central and southern United States. Hybridization rates vary substantially among populations in isolated drainage systems. We employed genome‐wide sampling to investigate geographic variation in hybridization, and to assess the possible importance of chromosome fusions to reproductive isolation among nine separate contact zones. The species differ by chromosomal rearrangements resulting from Robertsonian (Rb) fusions, so we hypothesized that Rb fusion chromosomes would serve as reproductive barriers, exhibiting steeper genomic clines than the rest of the genome. We observed variation in hybridization dynamics among drainages that ranged from nearly random mating to complete absence of hybridization. Contrary to predictions, our use of genomic cline analyses on mapped species‐diagnostic SNP markers did not indicate consistent patterns of variable introgression across linkage groups, or an association between Rb fusions and genomic clines that would be indicative of reproductive isolation. We did observe a relationship between hybridization rates and population phylogeography, with the lowest rates of hybridization tending to be found in populations inferred to have had the longest histories of drainage sympatry. Our results, combined with previous studies of contact zones between the species, support population history as an important factor in explaining variation in hybridization rates.

    more » « less
  3. Abstract

    Incompletely isolated species provide an opportunity to investigate the genetic mechanisms and evolutionary forces that maintain distinct species in the face of ongoing gene flow. Here, we use field surveys and reduced representation sequencing to characterize the patterns of reproductive isolation, admixture and genomic divergence between populations of the outcrossing wildflowerMimulus guttatusand selfingM. nasutus. Focusing on a single site where these two species have come into secondary contact, we find that phenological isolation is strong, although incomplete, and is likely driven by divergence in response to photoperiod. In contrast to previous field studies, which have suggested that F1‐hybrid formation might be rare, we discover patterns of genomic variation consistent with ongoing introgression. Strikingly, admixed individuals vary continuously from highly admixed to nearly pureM. guttatus, demonstrating ongoing hybridization and asymmetric introgression fromM. nasutusintoM. guttatus. Patterns of admixture and divergence across the genome show that levels of introgression are more variable than expected by chance. Some genomic regions show a reduced introgression, including one region that overlaps a critical photoperiodQTL, whereas other regions show elevated levels of interspecific gene flow. In addition, we observe a genome‐wide negative relationship between absolute divergence and the local recombination rate, potentially indicating natural selection againstM. nasutusancestry inM. guttatusgenetic backgrounds. Together, our results suggest thatMimulusspeciation is both ongoing and dynamic and that a combination of divergence in phenology and mating system, as well as selection against interspecific alleles, likely maintains these sympatric species.

    more » « less
  4. Abstract

    The paleback darter,Etheostoma pallididorsum, is considered imperilled and has recently been petitioned for listing under the Endangered Species Act. Previous allozyme‐based studies found evidence of a small effective population size, warranting conservation concern. The objective of this study was to assess the population dynamics and the phylogeographical history of the paleback darter, using a multilocus microsatellite approach and mitochondrial DNA.

    The predictions of this study were that: paleback darter populations will exhibit low genetic diversity and minimal gene flow; population structure will correspond to the river systems from which the samples are derived; reservoir dams impounding the reaches between the Caddo and Ouachita rivers would serve as effective barriers to gene flow; and the Caddo and Ouachita rivers are reciprocally monophyletic.

    Microsatellite DNA loci revealed significant structure among sampled localities (globalFst= 0.17,P< 0.001), with evidence of two distinct populations representing the Caddo and Ouachita rivers. However, Bayesian phylogeographical analyses resulted in three distinct clades: Caddo River, Ouachita River, and Mazarn Creek. Divergence from the most recent ancestor shared among the river drainages was estimated at 60 Kya. Population genetic diversity was relatively low (He= 0.65; mean alleles per locus,A= 6.26), but was comparable with the population genetic diversity found in the close relatives slackwater darter,Etheostoma boschungi(He= 0.65;A= 6.74), and Tuscumbia darter,Etheostoma tuscumbia(He= 0.57;A= 5.53).

    These results have conservation implications for paleback darter populations and can be informative for other headwater specialist species. Like other headwater species with population structuring and relatively low genetic diversity, the persistence of paleback darter populations is likely to be tied to the persistence and connectivity of local breeding and non‐breeding habitat. These results do not raise conservation concern for a population decline; however, the restricted distribution and endemic status of the species still renders paleback darter populations vulnerable to extirpation or extinction.

    more » « less
  5. Premise of the Study

    This investigation establishes the firstDNA‐sequence‐based phylogenetic hypothesis of species relationships in the coca family (Erythroxylaceae) and presents its implications for the intrageneric taxonomy and neotropical biogeography ofErythroxylum. We also identify the closest wild relatives and evolutionary relationships of the cultivated coca taxa.


    We focused our phylogenomic inference on the largest taxonomic section in the genusErythroxylum(ArcherythroxylumO.E.Schulz) using concatenation and gene tree reconciliation methods from hybridization‐based target capture of 427 genes.

    Key Results

    We show that neotropicalErythroxylumare monophyletic within the paleotropical lineages, yetArcherythroxylumand all of the other taxonomic sections from which we sampled multiple species lack monophyly. We mapped phytogeographic states onto the tree and found some concordance between these regions and clades. The wild speciesE. gracilipesandE. cataractarumare most closely related to the cultivatedE. cocaandE. novogranatense, but relationships within this “coca” clade remain equivocal.


    Our results point to the difficulty of morphology‐based intrageneric classification in this clade and highlight the importance of integrative taxonomy in future systematic revisions. We can confidently identifyE. gracilipesandE. cataractarumas the closest wild relatives of the coca taxa, but understanding the domestication history of this crop will require more thorough phylogeographic analysis.

    more » « less