Two Genetically Distinct Populations of Bobtail Squid, Euprymna scolopes, Exist on the Island of O'ahu

Abstract

Population structure of the endemic Hawaiian bobtail squid, Euprymna scolopes, was examined using both morphological and genetic data. Although allozyme polymorphism was negligible, measurements of eggs, juveniles, and adults, as well as genetic data sequences of mitochondrial cytochrome oxidase I, demonstrated highly significant population structuring between two populations found on the northeastern and southern coasts of the island of O'ahu. These data suggest that extremely low levels of gene flow occur among these populations. Population subdivision of marine shallow-water invertebrates in Hawai'i is not expected based on earlier surveys, but may reflect a more general pattern for organisms, both marine and terrestrial, that exhibit limited dispersal. The subdivision also provides insight into the pathway through which coevolution between E. scolopes and its internal symbiont, Vibrio fischeri, may proceed.

The Hawaiian Archipelago presents unique opportunities for the study of evolutionary biology because of its relative isolation, high levels of endemism, and the explosive radiation of a number of taxa (Simon 1987, Wagner and Funk 1995). For example, the terrestrial invertebrate biota, which has been particularly well studied in genera such as Drosophila flies, Tetragnatha spiders, and Achatinellinae tree snails, typically exhibits extensive adaptive radiations comprising species endemic to the archipelago (Roderick and Gillespie 1998, Thacker and Hadfield 2000). These patterns are thought to result from the extremely heterogeneous nature of the terrestrial island landscape, which presents an abundance of spatially limited, yet distinct, niches ripe for adaptive radiation (Gillespie et al. 2001).

Marine invertebrates, however, have much lower rates of endemism than their terrestrial counterparts, with endemism ranging from 2 to 20% for nearshore gastropods, brachyuran decapods, and certain polychaetes and echinoderms of the central Pacific (Scheltema 1986, Kay and Palumbi 1987). These benthic marine invertebrates appear instead to represent attenuated Indo-Pacific fauna, and the marine endemic species that do exist are usually distributed throughout all of the islands of the archipelago (Scheltema 1986). The wide geographic distributions of these marine invertebrate species indicate that fairly high gene flow must be occurring between populations within species (Palumbi 1992). Such gene flow is presumably facilitated by long planktonic larval phases, which ensure high dispersal. Yet, within such widespread species some population structure may nevertheless persist (Barber et al. 2000).

Although much is known about marine invertebrate species with extended larval life histories, less is understood about species that do not have broadly dispersing larval or juvenile stages. One such species is the bobtail squid, Euprymna scolopes, which is endemic to the Hawaiian Islands (Singley 1983). Female E. scolopes lay clutches of eggs on hard substrates in the shallow waters of the back reef. No true larval stages occur in this species (i.e., the juveniles hatch with a morphology and behavior very similar to those of the adult [Arnold et al. 1972]). Specifically, after a brief planktonic stage of hours to a few days, the juvenile squid take on the diel pattern of behavior characteristic of the species (i.e., they bury in the sand during the day and forage in the water column at night).

Previously, it was observed that E. scolopes is notable for its habitat loyalty, and it has been suggested that two reproductively isolated populations exist on northeastern and southern coasts of the island of O'ahu (Singley 1983). The E. scolopes-Vibrio fischeri association has become a model for animal-bacterial symbiosis and in particular the persistent colonization of animal epithelia by extracellular bacteria (McFall-Ngai and Ruby 1998). Recent studies of the squid-vibrio symbioses at the level of species have provided strong evidence for coevolution of the host and symbiont (Nishiguchi et al. 1998). Whether population subdivision of E. scolopes exists is critical to understanding the co-evolution of this species with its bacteria partners—how isolated are populations of E. scolopes and at what scale would population-specific strains of V. fischeri be expected to evolve? In this study we tested the hypothesis of population subdivision of E. scolopes with both morphological and genetic data. Our results indicate...