Genetic structure of Atlantic and Gulf of Mexico populations of sea bass, menhaden, and sturgeon: Influence of zoogeographic factors and life-history patterns

To assess the influence of zoogeographic factors and life-history parameters (effective population size, generation length, and dispersal) on the evolutionary genetic structure of marine fishes in the southeastern USA, phylogeographic patterns of mitochondrial DNA (mtDNA) were compared between disjunct Atlantic and Gulf of Mexico populations in three coastal marine fishes whose juveniles require an estuarine or freshwater habitat for development. Black sea bass (Centropristis striata), menhaden (Brevoortia tyrannus and B. patronus) and sturgeon (Acipenser oxyrhynchus) samples were collected between 1986 and 1988. All species showed significant haplotype frequency differences between the Atlantic and Gulf, but the magnitude and distribution of mtDNA variation differed greatly among these taxa: sea bass showed little within-region mtDNA polymorphism and a clear phylogenetic distinction between the Atlantic and Gulf; menhaden showed extensive within-region polymorphism and a paraphyletic relationship between Atlantic and Gulf populations; and sturgeon exhibited very low m O N A diversity both within regions and overall. Evolutionary effective sizes of the female populations (N:(e)) estimated from the mtDNA data ranged from N:(e) = 50 (Gulf of Mexico sturgeon) to N:(e) = 800 000 (Atlantic menhaden), and showed a strong rank-order agreement with the current-day census sizes of these species. The relationship between N:(e) and the estimated times of divergence (t) among mtDNA lineages (from conventional clock calibrations) predicts the observed phylogenetic distinction between Atlantic and Gulf sea bass, as well as the paraphyletic pattern in menhaden, provided the populations have been separated by the same long-standing zoogeographic barriers thought to have influenced other coastal taxa in the southeastern USA. However, vicariant scenarios alone cannot explain other phylogenetic aspects of the menhaden (and sturgeon) mtDNA data and, for these species, recent gene flow between the Atlantic and Gulf coasts is strongly implicated. These data are relevant to management and conservation issues for these species. * Please address all requests for reprints to Dr. J. C. Avise Introduction The geographic structure of any species is a product of both historical and contemporary gene flow (Slatkin 1987), and is likely to have been affected by such factors as geographic or ecologic impediments to movement and inherent dispersal capability. An important issue in evolutionary biology concerns whether general and predictable relationships exist between the phylogeographic structures of species and their environmental requirements and life-histories. For example, freshwater fishes tend to be physically confined to particular bodies of water, and their populations commonly exhibit extensive geographic population structure reflecting historical patterns of drainage isolation and coalescence (Bermingham and Avise 1986, Avise et al. 1987a). In contrast, many oceanic and reef-based marine organisms exhibit extensive movement as larvae and/or adults (Rosenblatt 1963, Scheltema 1971), and at least some surveyed species show relatively little population genetic structure over huge areas (Winans 1980, Graves et al. 1984, Shaklee 1984, Avise et al. 1986, Gyllensten 1986, Avise 1987). However, marine species themselves exhibit a great diversity of life-history patterns with respect to dispersal. For example, in species that lay demersal eggs (e.g. toadfish), or in anadromous species that reproduce in freshwater (e.g. salmon), long-distance gene flow must occur primarily through movements of sub-adults or adults. Conversely, gene flow in species that are benthic as adults (e.g. oysters) may occur exclusively via movement of pelagic gametes or larvae. Many species exhibit extensive movements both as pelagic larvae and adults (e.g. tuna), while in comparison others show limited movement at all life-history stages (e.g. horseshoe crabs). Phylogeographic patterns in coastal marine species may be intermediate between freshwater and pelagic marine types, because the potential for dispersal is tempered by habitat availability along a linear zoogeographic regime. The distributional limits of coastal species are typically defined by major geographic or hydrologic boundaries, such as at Cape Cod, Cape Hatteras, and the Florida peninsula along the east coast of the USA (Hilde372 B.W. Bowen and J. C. Avise: Phytogeography of southeastern marine fishes brand and Schroeder 1928, Bigelow and Schroeder 1953, Briggs 1974). The Florida peninsula is of special interest because it divides the temperate coastal fauna of the southeastern USA into Atlantic and Gulf of Mexico provinces (Hoese and Moore 1977). Warm, subtropical conditions extend northward to central Florida on both sides of the peninsula, and at the present time divide some elements of the temperate fauna into allopatric units. In general, coastal marine fishes (and many invertebrates) utilize near-shore or estuarine habitat as nursery grounds for larvae and juveniles. In contrast to pelagic or reef-based species, where reproduction often involves long-distance transport of larvae, such coastal species have developed strategies to minimize offshore transplant (and loss) of larvae (Checkley et al. 1988). Here we examine mitochondrial DNA (mtDNA) population structure in three temperate coastal marine fishes that require an estuarine or freshwater habitat for juvenile development. Mitochondrial DNA is especially useful for elucidating population structure because this non-recombining molecule evolves rapidly and provides character states whose phylogenetic relationships readily can be deduced (Brown et al. 1979, Wilson et al. 1985, Avise 1986, 1989, Moritz et al. 1987). The geographic distribution of branches in an intraspecific mtDNA phylogeny constitutes the maternal "phylogeographic" pattern of a species (Avise et al. 1987 a). Our major goals are to: (1) further assess the influence of historical geographic factors and life-history pattern on the genetic structure of the marine fauna of the southeastern US; (2) provide genetic data that may be of relevance to management and conservation decisions for these species; and (3) assess two additional, seldom-considered factors in phylogeographic outcomes the significance of differing effective population sizes and generation lengths on the distributions of gene lineages within and among populations. Taxonomy and life-history background