Biogeography plays a significant role in species’ dispersal, and in turn population structure, across the landscape. The North American katydid Neoconocephalus melanorhinus belongs to a genus with high mobility. Unlike other members of the genus, N. melanorhinus is a salt marsh specialist restricted to a narrow corridor along the Atlantic and Gulf coasts. In addition, their range crosses at least one known biogeographic barrier and possesses biogeographic characteristics of the stepping-stone as well as the hierarchical island model of dispersal. Using AFLP markers we searched for areas that conform to the predictions of isolation by distance and for areas of non-uniform increases in genetic variance, indicative of isolation by barrier. We found significant genetic differentiation between all twelve sampled sites. Isolation by distance was the predominant pattern of variation across their range. In addition, we saw possible evidence of two biogeographic barriers to gene flow, one at the Atlantic-Gulf divide and the other along the Gulf coast. We also observed a change in body size across the range. Body size, as measured by male hind femur length, correlated closely with latitude, a possible indication of differential selection across the species range.

Funding: This work was supported by a grant from the National Science Foundation ( www.nsf.gov ) received by JS (IOS 1146878). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Copyright: © 2017 Ney, Schul. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Introduction

The phylogeography of organisms, i.e. the distribution of genetic lineages of a species across landscapes [1], is strongly affected by their dispersal ability [2]. Isolation by distance (IBD) and isolation by barrier (IBB) are two common patterns found among numerous species and taxonomic groups [3]. Most species show dispersal limitations across some spatial scale [4], i.e. individuals cannot disperse across their entire species’ range during their lifetime. Such reduced dispersal can result in a pattern of uniformly increasing genetic variation with geographic distance (= IBD, [5]). Alternatively, IBB occurs if biogeographic barriers to dispersal reduce gene flow. This often leads to a pattern of genetic discontinuity, i.e. a non-uniform increase in genetic differentiation across the landscape [6]. While the difference between IBD and IBB is likely an artificial dichotomy, their study allows us to contemplate the relative importance that various factors play in shaping population structure.

A number of models explain the genetic structure resulting from different dispersal limitations [5, 6] such as distance or barriers. Within the stepping-stone model dispersal is limited by geographic distance and individuals disperse only between neighboring sites. In its most restricted form, sites fall along a line. Within this one-dimensional stepping-stone model, dispersal is limited to, at most, two adjacent sites. This produces a strong signature of IBD as gene flow decreases with distance along a narrow corridor [5, 7].

In an alternative model, the hierarchical island model, barriers between certain neighboring sites reduce the rate of dispersal and gene flow. This produces a non-uniform increase in genetic differentiation between these sites, the signature of IBB [6]. This divides the population structure into distinct subpopulations. Within subpopulations there is an assumption of little or no genetic differentiation (panmixia). This is the result of significant gene flow within, and reduced gene flow between, subpopulations. Unlike in the stepping-stone model, geographic distance does not play a role in this pattern of genetic differentiation.

Neoconocephalus is a diverse group of New World katydids with variation in habitat preference and species distributions [8]. All species are highly mobile with strong flying capabilities and adult life spans of several months (review in [8]). Most species occupy large ranges, some of which encompass much of the Midwestern and Eastern United States. The North American ranges of these species seem to show little population level genetic structure [9]. For example, N. bivocatus and N. robustus show a lack of genetic structure across more than 450 km of grassland habitat (G. Ney and J. Schul unpublished data).

Neoconocephalus melanorhinus is a habitat specialist found only in North American salt marshes along the Atlantic and Gulf coasts [10]. This preference results in a species distribution, unique among Neoconocephalus katydids, that is more than 2,000 km long, but no more than a few kilometers wide in most localities. This one-dimensional arrangement of populations, which is similar to those in a one-dimensional stepping-stone model, may limit dispersal to neighboring sites and reduce gene flow across the range. Neoconocephalus melanorhinus’ range also falls along several known biogeographic divides, including one dividing the range on either side of the Florida peninsula (Fig 1). This Atlantic-Gulf divide is a significant barrier to gene flow in many marine taxa found along the Southern United States coast [3, 11]. In addition, their range crosses numerous other geographic features, including estuaries, developed shoreline, and stretches of coastline lacking saltmarsh habitat, that could potentially function as biogeographic barriers. Neoconocephalus melanorhinus’ narrow range may decrease individuals’ ability to avoid barriers by going around them and result in greater genetic differentiation among subpopulations on either side.

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larger image TIFF original image Download: Fig 1. Map of collection localities. Shaded in area represents the hypothesized range of N. melanorhinus (modified from [12]) based on literature and collection records. Squares and * represent sites sampled only in 2015. The dashed line indicates the site of the hypothesized Atlantic-Gulf divide. https://doi.org/10.1371/journal.pone.0179361.g001

Here we describe the population genetic structure of N. melanorhinus, a highly mobile species, in a one-dimensional range, which possesses characteristics of both a stepping-stone and a hierarchical island model. We sampled from twelve locales across the range. Using molecular markers and statistical tools, we searched for areas that conform to the predictions of IBD and for areas with non-uniform increases in genetic variance indicative of IBB. We note the confounding effect signals of IBD and IBB may have and utilized tools that control for these effects. In addition, we collected measurements for body size to determine whether this phenotype co-varies with the observed pattern of genetic differentiation across N. melanorhinus’ range.