skip to main content

Attention:

The NSF Public Access Repository (NSF-PAR) system and access will be unavailable from 5:00 PM ET until 11:00 PM ET on Friday, June 21 due to maintenance. We apologize for the inconvenience.


Title: Population genomics of rapidly invading lionfish in the Caribbean reveals signals of range expansion in the absence of spatial population structure
Abstract

Range expansions driven by global change and species invasions may have significant genomic, evolutionary, and ecological implications. During range expansions, strong genetic drift characterized by repeated founder events can result in decreased genetic diversity with increased distance from the center of the historic range, or the point of invasion. The invasion of the Indo‐Pacific lionfish,Pterois volitans, into waters off the US East Coast, Gulf of Mexico, and Caribbean Sea provides a natural system to study rapid range expansion in an invasive marine fish with high dispersal capabilities. We report results from 12,759 single nucleotide polymorphism loci sequenced by restriction enzyme‐associated DNA sequencing for nineP. volitanssampling areas in the invaded range, including Florida and other sites throughout the Caribbean, as well as mitochondrial control region D‐loop data. Analyses revealed low to no spatially explicit metapopulation genetic structure, which is partly consistent with previous finding of little structure within ocean basins, but partly divergent from initial reports of between‐basin structure. Genetic diversity, however, was not homogeneous across all sampled sites. Patterns of genetic diversity correlate with invasion pathway. Observed heterozygosity, averaged across all loci within a population, decreases with distance from Florida while expected heterozygosity is mostly constant in sampled populations, indicating population genetic disequilibrium correlated with distance from the point of invasion. Using anFSToutlier analysis and a Bayesian environmental correlation analysis, we identified 256 and 616 loci, respectively, that could be experiencing selection or genetic drift. Of these, 24 loci were shared between the two methods.

 
more » « less
NSF-PAR ID:
10457561
Author(s) / Creator(s):
 ;  ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Ecology and Evolution
Volume:
9
Issue:
6
ISSN:
2045-7758
Page Range / eLocation ID:
p. 3306-3320
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Understanding the consequences of exotic diseases on native forests is important to evolutionary ecology and conservation biology because exotic pathogens have drastically altered US eastern deciduous forests.Cornus floridaL. (flowering dogwood tree) is one such species facing heavy mortality. Characterizing the genetic structure ofC. floridapopulations and identifying the genetic signature of adaptation to dogwood anthracnose (an exotic pathogen responsible for high mortality) remain vital for conservation efforts. By integrating genetic data from genotype by sequencing (GBS) of 289 trees across the host species range and distribution of disease, we evaluated the spatial patterns of genetic variation and population genetic structure ofC. floridaand compared the pattern to the distribution of dogwood anthracnose. Using genome‐wide association study and gradient forest analysis, we identified genetic loci under selection and associated with ecological and diseased regions. The results revealed signals of weak genetic differentiation of three or more subgroups nested within two clusters—explaining up to 2%–6% of genetic variation. The groups largely corresponded to the regions within and outside the eastern Hot‐Continental ecoregion, which also overlapped with areas within and outside the main distribution of dogwood anthracnose. The fungal sequences contained in the GBS data of sampled trees bolstered visual records of disease at sampled locations and were congruent with the reported range ofDiscula destructiva, suggesting that fungal sequences within‐host genomic data were informative for detecting or predicting disease. The genetic diversity between populations at diseased vs. disease‐free sites across the range ofC. floridashowed no significant difference. We identified 72 single‐nucleotide polymorphisms (SNPs) from 68 loci putatively under selection, some of which exhibited abrupt turnover in allele frequencies along the borders of the Hot‐Continental ecoregion and the range of dogwood anthracnose. One such candidate SNP was independently identified in two prior studies as a possible L‐type lectin‐domain containing receptor kinase. Although diseased and disease‐free areas do not significantly differ in genetic diversity, overall there are slight trends to indicate marginally smaller amounts of genetic diversity in disease‐affected areas. Our results were congruent with previous studies that were based on a limited number of genetic markers in revealing high genetic variation and weak population structure inC. florida.

     
    more » « less
  2. Abstract

    Lemurs are among the world's most threatened mammals. The critically endangered black‐and‐white ruffed lemur (Varecia variegata), in particular, has recently experienced rapid population declines due to habitat loss, ecological sensitivities to habitat degradation, and extensive human hunting pressure. Despite this, a recent study indicates that ruffed lemurs retain among the highest levels of genetic diversity for primates. Identifying how this diversity is apportioned and whether gene flow is maintained among remnant populations will help to diagnose and target conservation priorities. We sampled 209 individuals from 19 sites throughout the remainingV. variegatarange. We used 10 polymorphic microsatellite loci and ~550 bp of mtDNAsequence data to evaluate genetic structure and population dynamics, including dispersal patterns and recent population declines. Bayesian cluster analyses identified two distinct genetic clusters, which optimally partitioned data into populations occurring on either side of theMangoro River. Localities north of the Mangoro were characterized by greater genetic diversity, greater gene flow (lower genetic differentiation) and higher mtDNAhaplotype and nucleotide diversity than those in the south. Despite this, genetic differentiation across all sites was high, as indicated by high averageFST(0.247) and ΦST(0.544), and followed a pattern of isolation‐by‐distance. We use these results to suggest future conservation strategies that include an effort to maintain genetic diversity in the north and restore connectivity in the south. We also note the discordance between patterns of genetic differentiation and current subspecies taxonomy, and encourage a re‐evaluation of conservation management units moving forward.

     
    more » « less
  3. Abstract

    The importance of genetic drift in shaping patterns of adaptive genetic variation in nature is poorly known. Genetic drift should drive partially recessive deleterious mutations to high frequency, and inter‐population crosses may therefore exhibit heterosis (increased fitness relative to intra‐population crosses). Low genetic diversity and greater genetic distance between populations should increase the magnitude of heterosis. Moreover, drift and selection should remove strongly deleterious recessive alleles from individual populations, resulting in reduced inbreeding depression. To estimate heterosis, we crossed 90 independent line pairs ofArabidopsis thalianafrom 15 pairs of natural populations sampled across Fennoscandia and crossed an additional 41 line pairs from a subset of four of these populations to estimate inbreeding depression. We measured lifetime fitness of crosses relative to parents in a large outdoor common garden (8,448 plants in total) in central Sweden. To examine the effects of genetic diversity and genetic distance on heterosis, we genotyped parental lines for 869 SNPs. Overall, genetic variation within populations was low (median expected heterozygosity = 0.02), and genetic differentiation was high (medianFST = 0.82). Crosses between 10 of 15 population pairs exhibited significant heterosis, with magnitudes of heterosis as high as 117%. We found no significant inbreeding depression, suggesting that the observed heterosis is due to fixation of mildly deleterious alleles within populations. Widespread and substantial heterosis indicates an important role for drift in shaping genetic variation, but there was no significant relationship between fitness of crosses relative to parents and genetic diversity or genetic distance between populations.

     
    more » « less
  4. Abstract Aim

    Patterns of genetic diversity within species’ ranges can reveal important insights into effects of past climate on species’ biogeography and current population dynamics. While numerous biogeographic hypotheses have been proposed to explain patterns of genetic diversity within species’ ranges, formal comparisons and rigorous statistical tests of these hypotheses remain rare. Here, we compared seven hypotheses for their abilities to describe the geographic pattern of two metrics of genetic diversity in balsam poplar (Populus balsamifera), a northern North American tree species.

    Location

    North America.

    Taxon

    Balsam poplar (Populus balsamiferaL.).

    Methods

    We compared seven hypotheses, representing effects of past climate and current range position, for their ability to describe the geographic pattern of expected heterozygosity and per cent polymorphic loci across 85 populations of balsam poplar. We tested each hypothesis using spatial and non‐spatial least‐squares regression to assess the importance of spatial autocorrelation on model performance.

    Results

    We found that both expected heterozygosity and per cent polymorphic loci could best be explained by the current range position and genetic structure of populations within the contemporary range. Genetic diversity showed a clear gradient of being highest near the geographic and climatic range centre and lowest near range edges. Hypotheses accounting for the effects of past climate (e.g. past climatic suitability, distance from the southern edge), in contrast, had comparatively little support. Model ranks were similar among spatial and non‐spatial models, but residuals of all non‐spatial models were significantly autocorrelated, violating the assumption of independence in least‐squares regression.

    Main conclusions

    Our work adds strong support for the “Central‐Periphery Hypothesis” as providing a predictive framework for understanding the forces structuring genetic diversity across species’ ranges, and illustrates the value of applying a robust comparative model selection framework and accounting for spatial autocorrelation when comparing biogeographic models of genetic diversity.

     
    more » « less
  5. Abstract Biological introductions are unintended “natural experiments” that provide unique insights into evolutionary processes. Invasive phytophagous insects are of particular interest to evolutionary biologists studying adaptation, as introductions often require rapid adaptation to novel host plants. However, adaptive potential of invasive populations may be limited by reduced genetic diversity—a problem known as the “genetic paradox of invasions”. One potential solution to this paradox is if there are multiple invasive waves that bolster genetic variation in invasive populations. Evaluating this hypothesis requires characterizing genetic variation and population structure in the invaded range. To this end, we assemble a reference genome and describe patterns of genetic variation in the introduced white pine sawfly, Diprion similis. This species was introduced to North America in 1914, where it has rapidly colonized the thin-needled eastern white pine (Pinus strobus), making it an ideal invasion system for studying adaptation to novel environments. To evaluate evidence of multiple introductions, we generated whole-genome resequencing data for 64 D. similis females sampled across the North American range. Both model-based and model-free clustering analyses supported a single population for North American D. similis. Within this population, we found evidence of isolation-by-distance and a pattern of declining heterozygosity with distance from the hypothesized introduction site. Together, these results support a single-introduction event. We consider implications of these findings for the genetic paradox of invasion and discuss priorities for future research in D. similis, a promising model system for invasion biology. 
    more » « less