Range-wide population genetic structure of the Caribbean marine angiosperm Thalassia testudinum - PubMed (original) (raw)

. 2018 Aug 29;8(18):9478-9490.

doi: 10.1002/ece3.4443. eCollection 2018 Sep.

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Range-wide population genetic structure of the Caribbean marine angiosperm Thalassia testudinum

Kor-Jent van Dijk et al. Ecol Evol. 2018.

Abstract

Many marine species have widespread geographic ranges derived from their evolutionary and ecological history particularly their modes of dispersal. Seagrass (marine angiosperm) species have ranges that are unusually widespread, which is not unexpected following recent reviews of reproductive strategies demonstrating the potential for long-distance dispersal combined with longevity through clonality. An exemplar of these dual biological features is turtle grass (Thalassia testudinum) which is an ecologically important species throughout the tropical Atlantic region. Turtle grass has been documented to have long-distance dispersal via floating fruits and also extreme clonality and longevity. We hypothesize that across its range, Thalassia testudinum will have very limited regional population structure due to these characteristics and under typical models of population structure would expect to detect high levels of genetic connectivity. There are very few studies of range-wide genetic connectivity documented for seagrasses or other sessile marine species. This study presents a population genetic dataset that represents a geographic area exceeding 14,000 km2. Population genetic diversity was evaluated from 32 Thalassia testudinum populations sampled across the Caribbean and Gulf of Mexico. Genotypes were based on nine microsatellites, and haplotypes were based on chloroplast DNA sequences. Very limited phylogeographic signal from cpDNA reduced the potential comparative analyses possible. Multiple analytical clustering approaches on population genetic data revealed two significant genetic partitions: (a) the Caribbean and (b) the Gulf of Mexico. Genetic diversity was high (H E = 0.641), and isolation by distance was significant; gene flow and migration estimates across the entire range were however modest, we suggest that the frequency of successful recruitment across the range is uncommon. Thalassia testudinum maintains genetic diversity across its entire distribution range. The genetic split may be explained by genetic drift during recolonization from refugia following relatively recent reduction in available habitat such as the last glacial maxima.

Keywords: Gulf of Mexico; gene flow; genetic differentiation; long‐distance dispersal; seagrass; turtle grass.

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Figures

Figure 1

Figure 1

Populations of Thalassia testudinum and phylogeographic assignment. Collection sites of 32 T. testudinum populations in its total distribution range (edge delimited by solid line). Population details are found in Supporting Information Table S1 in Appendix S2. Each pie depicts the relative assignment proportions of each population to clusters 1 and 2 (Caribbean and Gulf of Mexico). The diameter of each pie corresponds to the population's relative allelic diversity (Table 1). Within each pie, the attribution to rbcLa haplotype C or T is also shown. The gray arrows show the directions and intensities of the major superficial currents (Gyory, Mariano, & Ryan, 2005)

Figure 2

Figure 2

Isolation by distance for Thalassia testudinum. Isolation by distance (IBD) was calculated for populations of Thalassia testudinum through the whole range (Graphs a–c**)**. Based on genetic assignments with Structure, IBD was also calculated within each cluster (Caribbean (d–f) and Gulf of Mexico (g–i)). Populations sharing assignments to both clusters were included in both datasets if assignment proportions were between 0.3 and 0.7 (Supporting Information Table S3 in Appendix S1). Correlations were based on pairwise genetic distance as F ST (Weir & Cockerham, 1984), pairwise standardized FST′ (Hedrick, 2005; Jost, 2008), and Jost's D EST (Jost, 2008) against the pairwise geographic distance (determined by de shortest distance over water possible; see Supporting Information Tables S3–S11 in Appendix S2). Log‐geographic corrections were applied to all analyses according to Rousset (1997)

Figure 3

Figure 3

Connectivity graph of 32 populations of Thalassia testudinum in the Caribbean and the Gulf of Mexico. Relative migration between populations pairs for all 32 populations was calculated and plotted with the R package diveRsity (Keenan et al., 2013) using the divMigrate function (Sundqvist, Zackrisson, & Kleinhans, 2013) and using Nm^ (Alcala et al., 2014) as the connectivity (migration) estimate (Supporting Information Table S13 in Appendix S2). The divMigrate function plots the relative asymmetric migration between populations, from microsatellite allele frequency data. A lower threshold of relative migration of 0.14 was used to eliminate uninformative edges, and edges were scaled by width and color saturation when above 0.40. Wider and darker edges represent the most connected sites of this study with the highest relative connectivity (1.0) between 23.US Craig Key and 24.US Arsenicker. The numbers within the nodes represent the populations as in Table 1

References

    1. Alberto, F. , Massa, S. , Manent, P. , Díaz‐Almela, E. , Arnaud‐Haond, S. , Duarte, C. M. , & Serrão, E. A. (2008). Genetic differentiation and secondary contact zone in the seagrass Cymodocea nodosa across the Mediterranean‐Atlantic transition region. Journal of Biogeography, 35, 1279–1294. 10.1111/j.1365-2699.2007.01876.x -DOI
    1. Alcala, N. , Goudet, J. , & Vuilleumier, S. (2014). On the transition of genetic differentiation from isolation to panmixia: What we can learn from Gst and D. Theoretical Population Biology, 93, 75–84. 10.1016/j.tpb.2014.02.003 -DOI -PubMed
    1. Arnaud‐Haond, S. , & Belkhir, K. (2007). GENCLONE: A computer program to analyse genotypic data, test for clonality and describe spatial clonal organization. Molecular Ecology Notes, 7, 15–17.
    1. Arnaud‐Haond, S. , Duarte, C. M. , Alberto, F. , & Serrão, E. A. (2007). Standardizing methods to address clonality in population studies. Molecular Ecology, 16, 5115–5139. 10.1111/j.1365-294X.2007.03535.x -DOI -PubMed
    1. Arnaud‐Haond, S. , Duarte, C. M. , Diaz‐Almela, E. , Marba, N. , Sintes, T. , & Serrao, E. A. (2012). Implications of extreme life span in clonal organisms: Millenary clones in meadows of the threatened seagrass Posidonia oceanica . PLoS ONE, 7, e30454 10.1371/journal.pone.0030454 -DOI -PMC -PubMed

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