Molecular Evidence for Cryptic Species ofAurelia aurita(Cnidaria, Scyphozoa)

Abstract

Morphological taxonomy suggests that marine faunas are species poor compared to terrestrial and freshwater faunas (1). This dichotomy has been attributed to the unique potential of marine plankters for distant dispersal across homogenous oceans with few barriers to gene flow (2). The relative scarcity of opportunities for allopatric divergence has resulted in depauperate marine faunas characterized by a high proportion of widespread or cosmopolitan species. Aurelia aurita (Linnaeus) has been considered a good example of such a cosmopolite (3, 4, 5, 6). However, recent molecular studies have revealed cryptic species in many marine taxa (7), suggesting that marine biodiversity is higher and opportunities for speciation have been more frequent than generally recognized. Here, we present nuclear and mitochondrial DNA sequence evidence of seven sibling species of Aurelia aurita and two additional species, A. limbata Brandt and A. labiata Chamisso & Eysenhardt. These sequence data indicate speciation events as early as the late Cretaceous or early Tertiary, consistent with the formation of well-recognized biogeographic barriers to gene flow in the seas. Traditionally, the genus Aurelia comprises two species: A. limbata, a polar species, and A. aurita, a common inhabitant of nearshore waters circumglobally between about 50 °N and 55 °S (3, 4, 5; Fig. 1). Perhaps due to its ubiquity, A. aurita has become a popular research organism for studies as diverse as protein chemistry, development, ecology, ethology, and hydrodynamics (6). A. aurita also is economically important because worldwide it preys on or competes with larvae of commercial fisheries and because swarms of medusae may impede trawling or block power-plant intakes (8). Furthermore, this “pest” has been introduced at least into San Francisco Bay (9) and possibly many other places (10). A. aurita is also familiar to nonspecialists because it is the most commonly displayed medusa in public aquaria. The systematics of A. aurita therefore is of considerable scientific, economic, and general interest. Aurelia has a typical bipartite scyphozoan life history in which benthic scyphopolyps asexually strobilate ephyrae that grow into sexual medusae, the females of which brood larvae that settle into the shallow coastal benthos within a few days of being released. Of these life stages, the medusa probably is the principal dispersal phase because only the medusa is both long-lived (several months to more than one year; 11) and planktonic (6). The potential of medusae for distant dispersal is consistent with the current classification of A. aurita as a circumglobal, almost cosmopolitan, species (4, 5). However, A. aurita medusae in Saanich Inlet, British Columbia, and perhaps elsewhere, migrate directionally (12), maintaining breeding aggregations within isolated inlets and probably limiting gene flow among populations. Consistent with limited gene flow, allozyme differences have been found between populations of A. aurita in the eastern and western Atlantic Ocean, the Gulf of Mexico, and the eastern and western Pacific Ocean (9, 13). In addition, one species, A. labiata, was recently recognized as native to Pacific North America and distinct from A. aurita (10). Novel DNA sequence data from nuclear internal transcribed spacer one (ITS-1) and mitochondrial cytochrome oxidase c subunit I (COI) reveal highly structured gene genealogies and at least nine distinct clades of Aurelia (Figs. 1, 2). Several lines of argument suggest that these clades warrant recognition as distinct species. First, the length of ITS-1 varies from 240 nucleotides (Charlestown, RI) to 360 nucleotides (Cananeia, Brazil). Such length variation is comparable to that found among congeneric species of Received 7 August 2000; accepted 19 October 2000. * To whom correspondence should be addressed at Coral Reef Research Foundation, Box 1765, Koror, PW 96940, Palau. Reference: Biol. Bull. 200: 92–96. (February 2001)