Population genomics reveals multiple drivers of population differentiation in a sex‐role‐reversed pipefish

Abstract

A major goal of molecular ecology is to identify the causes of genetic and phenotypic differentiation among populations. Population genomics is suitably poised to tackle these key questions by diagnosing the evolutionary mechanisms driving divergence in nature. Here, we set out to investigate the evolutionary processes underlying population differentiation in the Gulf pipefish, Syngnathus scovelli. We sampled approximately 50 fish from each of 12 populations distributed from the Gulf coast of Texas to the Atlantic coast of Florida and performed restriction-site-associated DNA sequencing to identify SNPs throughout the genome. After imposing quality and stringency filters, we selected a panel of 6348 SNPs present in all 12 populations, 1753 of which were not physically linked. We identified a genome-wide pattern of isolation by distance, in addition to a more substantial genetic break separating populations in the Gulf of Mexico from those in the Atlantic. We also used several divergence outlier approaches and tests for genotype-environment correlations to identify 400 SNPs putatively involved in local adaptation. Patterns of phenotypic differentiation and variation diverged from the overall genomic pattern, suggesting that selection, phenotypic plasticity or demographic factors may be shaping phenotypes in distinct populations. Overall, our results suggest that population divergence is driven by a variety of factors in S. scovelli, including neutral processes and selection on multiple traits.

Substantial differences in bias between single‐digest and double‐digest RAD‐seq libraries: A case study

“…If coverage filters were not in place, the F ST values ranged up to 0.9788 when the two types of libraries were analysed together and 0.4883 when analysed separately. These extreme values were much larger than the maximum values observed between geographically distinct populations of S. scovelli (Flanagan et al, 2016). The difference between genotyping methods was not simply due to the fact that we sampled 60 individuals using sdRAD-seq and 384 using ddRAD-seq, because a comparison of 60 randomly selected ddRAD individuals to the 60 sdRAD individuals yielded F ST values that were substantially higher than a comparison of 60 ddRAD individuals to another 60 ddRAD individuals ( Figure 3).…”

“…We followed the ddRAD‐seq library preparation method from Peterson et al. () with several modifications described elsewhere (Flanagan & Jones, ; Flanagan, Rose, & Jones, ). Briefly, 1 μg of genomic DNA from each individual was digested with 100 units of Pst I ‐ HF (New England Biolabs) and 25 units of Mbo I (New England Biolabs) in a 3‐hr, 37°C incubation.…”

“…We prepared four ddRAD-seq libraries containing a total of 159 pregnant males, eight nonpregnant males, 160 offspring and 57 females (384 individuals total). We followed the ddRAD-seq library preparation method from Peterson et al (2012) with several modifications described elsewhere (Flanagan & Jones, 2017;Flanagan, Rose, & Jones, 2016). Briefly, 1 lg of genomic DNA from each individual was digested with 100 units of PstI-HF (New England Biolabs) and 25 units of MboI (New England Biolabs) in a 3-hr, 37°C incubation.…”

Artificial Selection to Increase the Phenotypic Variance ingmaxFails

“…Correlated Responses to Selection. A direct way to identify the multivariate traits that had experienced the greatest change in phenotypic variance throughout the selection experiment was to use a fourth-order covariance tensor (Σ P ) that characterized the variation among the phenotypic covariance matrices within each of the two treatments of the experiment (see the appendix; Hine et al 2009;Robinson and Beckerman 2013;Aguirre et al 2014;Walsh 2014;Careau et al 2015;Flanagan et al 2016). The fourth-order covariance tensor (Σ P ) characterizes the variances and covariances among matrices, analogous to how a P matrix (a second-order tensor) characterizes the variances and covariances among traits.…”

Phylogeography of sand‐burrowing amphipods (Haustoriidae) supports an ancient suture zone in the Gulf of Mexico

“…For example, a hybrid zone suspected to reflect secondary contact between species of Menippe crabs lies along northern Florida and into Mobile Bay, Alabama (Bert, 1986). Other sister species or populations appear divided on either side of the Mississippi River, such as the lane snapper (Lutjanus synagris; Portnoy & Gold, 2012), Gulf squid (Loligo plei ;Herke & Foltz, 2002) and the dusky pipefish (Syngnathus scovelli; Flanagan, Rose, & Jones, 2016). A second issue arises in that the timing of divergence is not the same across these sister groups, indicating there were likely multiple vicariant events in the Gulf of Mexico periodically throughout the history of the basin (Avise, 1992).…”