Evolutionary associations between sand seatrout (Cynoscion arenarius) and silver seatrout (C. nothus) inferred from morphological characters, mitochondrial DNA, and microsatellite markers Item Type article Authors Anderson, Joel D.; McDonald, Dusty L.; Sutton, Glen R.; Karel, William J. Download date 23/09/2021 08:57:20 Link to Item http://hdl.handle.net/1834/25457 13 Abstract—The evolutionary asso- ciations between closely related fish Evolutionary associations between sand seatrout species, both contemporary and his- (Cynoscion arenarius) and silver seatrout torical, are frequently assessed by using molecular markers, such as (C. nothus) inferred from morphological characters, microsatellites. Here, the presence mitochondrial DNA, and microsatellite markers and variability of microsatellite loci in two closely related species of marine fishes, sand seatrout (Cynoscion are- Joel D. Anderson (contact author)1 narius) and silver seatrout (C. nothus), Dusty L. McDonald1 are explored by using heterologous primers from red drum (Sciaenops Glen R. Sutton2 ocellatus). Data from these loci are William J. Karel1 used in conjunction with morphologi- cal characters and mitochondrial DNA Email address for contact author: [email protected] haplotypes to explore the extent of 1 Perry R. Bass Marine Fisheries Research Station genetic exchange between species off- Texas Parks and Wildlife Department shore of Galveston Bay, TX. Despite HC02 Box 385, Palacios, Texas 77465 seasonal overlap in distribution, low 2 Galveston Bay Field Office genetic divergence at microsatellite Texas Parks and Wildlife Department loci, and similar life history param- 1502 FM 517 East, eters of C. arenarius and C. nothus, all Dickinson, Texas 77539 three data sets indicated that hybrid- ization between these species does not occur or occurs only rarely and that historical admixture in Galveston Bay after divergence between these species was unlikely. These results The molecular genetic associations species (C. arenarius, C. nothus, spot- shed light upon the evolutionary his- tory of these fishes and highlight the between populations of sand seatrout ted seatrout [C. nebulosus], and gray genetic properties of each species that (Cynoscion arenarius) and silver seat- weakfish [C. regalis]). Although these are influenced by their life history rout (C. nothus) have not been specifi- methods provided some insight into and ecology. cally examined on a large scale with the evolutionary relationships among DNA methods despite the close ties the species, the data of Weinstein between the respective fisheries for and Yerger (1976) were insufficient the two species. In particular, the pos- to answer direct questions about rates sibility of contemporary hybridization of contemporary and recent historical or historical admixture between these gene flow within and among Cynoscion species remains to be explored by species. Enzyme electrophoresis has using a large panel of unlinked DNA since been superceded by DNA-based markers. Sand and silver seatrout are methods on a broad scale. Microsatel- so morphologically similar that they lite markers are likely more sensitive are collectively known as white trout for studies involving high rates of gene by fishermen (Ginsburg, 1931). Both flow and low levels of population iden- species are abundant throughout the tity (Wright and Bentzen, 1994). This Gulf of Mexico (hereafter, GOM); the is particularly true for marine fishes, distribution range for sand seatrout whose populations are often charac- extends into the Atlantic Ocean, north terized by enormous census sizes and to Georgia, and the distribution range higher rates of migration between for silver trout extends to Massachu- subpopulations than freshwater and setts (Hildebrand and Schroeder, 1928; terrestrial organisms (DeWoody and Cordes and Graves, 2003). These seat- Avise, 2000). rout make up a modest proportion of Previous morphological compari- bycatch in shrimp and other commer- sons of sand and silver seatrout have cial trawl operations (Warren, 1981), resulted in a suite of distinct charac- although commercial landings have teristics that vary between species in Manuscript submitted 24 April 2008. Manuscript accepted 22 August 2008. decreased dramatically in the last 30 larval (Ditty, 1989) and adult stages Fish. Bull. 107:13–23 (2009). years (Fig. 1). Weinstein and Yerger (Ginsburg, 1929, 1931; Gunter, 1945; (1976) completed perhaps the most Moshin, 1973; Chao, 2002). However, The views and opinions expressed comprehensive study of molecular evo- both display a similar streamlined or implied in this article are those lution in the genus Cynoscion; they and fusiform body shape, and the of the author and do not necessarily reflect the position of the National assessed protein electrophoresis vari- ranges of numerous commonly used Marine Fisheries Service, NOAA. ants in all four western North Atlantic morphometric and meristic measures 14 Fishery Bulletin 107(1) overlap between the species. Addition- ally, hybridization, regional differentia- 900 tion, or a combination of both, may often 800 confound the trademark diagnostics used 700 to distinguish between the two species. 600 In any event, the superficial similarity ic tons) of these species indicates that morpho- 500 logical divergence has been minimal 400 and the concurrent bimodal timing of 300 spawning indicates overlapping life his- 200 tory parameters (Sheridan et al., 1984). Landings (metr 100 Distributional data seem to indicate that these species exhibit some habitat par- 0 1976 1981 1986 1991 1996 2001 2006 titioning (primarily by water depth and distance from the shore) with the re- Figure 1 sult that silver seatrout are found more Commercial landings (in metric tons) of white trout (Cynoscion nothus frequently in deeper water farther from and C. arenarius combined), from 1976 to 2006. Data provided by the shore (Ginsburg, 1931; Byers, 1981). Office of Science and Technology, National Marine Fisheries Service, These life history and distributional Silver Spring, MD, 2007. data yield a framework for devising hy- potheses to test the influence of niche overlap on historical associations be- tween sand and silver seatrout populations. In par- lite genotypes should be more reliable than assignment ticular, if hybridization between these species occurs, it by means of mtDNA haplotypes if mtDNA lineages is likely to occur in areas of contact such as nearshore have not been sorted categorically into contemporary marine waters used commonly by both species. Hy- populations (species). Third, in the case of no gene bridization in the genus Cynoscion has been previously flow between the species, microsatellite assignment documented on the Atlantic coast of Florida (Cordes should be conclusive, mtDNA haplotypes should sort and Graves, 2003). In their initial examinations, Cordes conclusively by species, and specimens should not reveal and Graves (2003) characterized populations of gray morphological intermediates for characters previously weakfish using genetic techniques and in doing so also described as diagnostic among species. Each of these identified putative hybrids between gray weakfish and competing hypotheses was examined in light of evidence either sand or silver seatrout. This identification was from the three data sets. The morphological and genetic accomplished by using four microsatellite markers and similarities and differences between the species were two nuclear intron gene regions (restriction fragment examined as evidence for hybridization, and as an aid length polymorphisms, or RFLP’s). Although these for future species identification. Finally, aspects of the markers were appropriate for identification of hybrids ecology and life history of each species are invoked to with gray weakfish, they were ineffective for determin- explain the patterns of genetic variability within and ing conclusively whether the second gametic contribu- between these congeneric species. tion was made by sand or silver seatrout. Here, both morphological and molecular (nuclear mi- crosatellites and mitochondrial restriction fragments) Materials and methods data are used to characterize populations of sand and silver seatrout from the nearshore Gulf waters outside Sample collection and laboratory methods of Galveston Bay, Texas. Three competing hypotheses regarding genetic associations between these species are In July of 2007, whole fish were collected offshore of evaluated. First, in the case of contemporary hybridiza- Galveston Bay, TX, during annual routine monitoring by tion, hybrids would appear as proportionate admixtures the Texas Parks and Wildlife, Coastal Fisheries Division. of both parental forms in microsatellite assignment White trout were collected with a 5.7-m otter trawl with tests. Moreover, the directionality of hybridization could 38-mm nylon multifilament mesh stretched throughout. be assessed with the use of mtDNA haplotypes (Wirtz, Trawl tows (n=4) were conducted parallel to the fathom 1999), and hybrids would likely be found to be interme- curve at a speed of three mph for ten minutes (Fig. 2). diate for diagnostic morphological characters (Hubbs, After collection, fish were frozen and transported to the 1955; Campton, 1987). Second, in the case of historical Perry R. Bass Marine Fisheries Research Station in association, such as lineage overlap during speciation or Palacios, Texas, for processing. lineage admixture after speciation, mtDNA haplotypes The sample consisted of 60 young adult sand seat- might be