Abstract
The adaptive radiation of the seven‐spined gobies (Gobiidae: Gobiosomatini) represents a classic example of how ecological specialization and larval retention can drive speciation through local adaptation. However, geographically widespread and phenotypically uniform species also do occur within Gobiosomatini. This lack of phenotypic variation across large geographic areas could be due to recent colonization, widespread gene flow, or stabilizing selection acting across environmental gradients. We use a phylogeographic approach to test these alternative hypotheses in the naked goby Gobiosoma bosc, a widespread and phenotypically invariable intertidal fish found along the Atlantic Coast of North America. Using DNA sequence from 218 individuals sampled at 15 localities, we document marked intraspecific genetic structure in mitochondrial and nuclear genes at three main geographic scales: (i) between Gulf of Mexico and Atlantic Coast, (ii) between the west coast of the Florida peninsula and adjacent Gulf of Mexico across the Apalachicola Bay, and (iii) at local scales of a few hundred kilometers. Clades on either side of Florida diverged about 8 million years ago, whereas some populations along the East Cost show divergent phylogroups that have differentiated within the last 200,000 years. The absence of noticeable phenotypic or ecological differentiation among lineages suggests the role of stabilizing selection on ancestral phenotypes, together with isolation in allopatry due to reduced dispersal and restricted gene flow, as the most likely explanation for their divergence. Haplotype phylogenies and spatial patterns of genetic diversity reveal frequent population bottlenecks followed by rapid population growth, particularly along the Gulf of Mexico. The magnitude of the genetic divergence among intraspecific lineages suggests the existence of cryptic species within Gobiosoma and indicates that modes of speciation can vary among lineages within Gobiidae.
Highlights
Recent research into diversification mechanisms in marine organisms using molecular data has revealed that pelagic larval stages, once thought to homogenize gene pools and prevent divergence, are often characterized by high levels of local recruitment (Barber, Palumbi, Erdmann, & Moosa, 2002; Jones, Milicich, Emslie, & Lunow, 1999; Swearer, Caselle, Lea, & Warner, 1999; Taylor & Hellberg, 2003), providing high potential for reduced gene flow and local adaptation (Bernardi, 2013)
The magnitude of the genetic divergence among intraspecific lineages suggests the existence of cryptic species within Gobiosoma and indicates that modes of speciation can vary among lineages within Gobiidae
Even within groups like the seven-spined gobies, characterized by highly ecologically specialized species assemblages at small geographic scales, some species stand out for showing no apparent phenotypic differentiation across large geographic ranges. Such is the case of the naked goby (Gobiosoma bosc Lacepède, 1800), a species found in shallow estuarine habitats, which shows what appears to be a complete lack of phenotypic differentiation across its large geographic distribution, which spans the Atlantic Coast of North America, from the state of New York in the North East, down through the Florida peninsula and along the Gulf Coast to the state of Texas
Summary
Recent research into diversification mechanisms in marine organisms using molecular data has revealed that pelagic larval stages, once thought to homogenize gene pools and prevent divergence, are often characterized by high levels of local recruitment (Barber, Palumbi, Erdmann, & Moosa, 2002; Jones, Milicich, Emslie, & Lunow, 1999; Swearer, Caselle, Lea, & Warner, 1999; Taylor & Hellberg, 2003), providing high potential for reduced gene flow and local adaptation (Bernardi, 2013). Such is the case of the naked goby (Gobiosoma bosc Lacepède, 1800), a species found in shallow estuarine habitats, which shows what appears to be a complete lack of phenotypic differentiation across its large geographic distribution, which spans the Atlantic Coast of North America, from the state of New York in the North East, down through the Florida peninsula and along the Gulf Coast to the state of Texas This apparent lack of geographically structured phenotypic variability can take place even at oceanic or continental scales and could be due to three main causes: (i) recent colonization across large areas, with insufficient time for lineage sorting and divergence; (ii) ongoing gene flow at regional or oceanic scales associated with pelagic larval stages, which may homogenize gene pools and prevent differentiation; and (iii) strong balancing selection on ancestral phenotypic traits despite local differences in ecological conditions. We used relationships among haplotypes and their relative frequencies to infer the historical demography of different populations of the species across its distribution
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