High Gene Flow Due to Pelagic Larval Dispersal Among South
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Heredity (2010) 104, 563–572 & 2010 Macmillan Publishers Limited All rights reserved 0018-067X/10 $32.00 www.nature.com/hdy ORIGINAL ARTICLE High gene flow due to pelagic larval dispersal among South Pacific archipelagos in two amphidromous gastropods (Neritomorpha: Neritidae) ED Crandall, JR Taffel and PH Barber1 Department of Biology, Boston University Marine Program, Boston, MA, USA The freshwater stream fauna of tropical oceanic islands is have a pelagic larval duration (PLD) of at least 8 weeks, dominated by amphidromous species, whose larvae are longer than many marine species. In addition, the two species transported to the ocean and develop in the plankton before have recently colonized isolated Central Pacific archipelagos recruiting back to freshwater habitat as juveniles. Because in three independent events. Since colonization, there has stream habitat is relatively scarce and unstable on oceanic been little or no gene flow between the Western and Central islands, this life history would seem to favor either the Pacific archipelagos in N. canalis, and high levels of gene retention of larvae to their natal streams, or the ability to flow across the same region in N. dilatatus. Both species delay metamorphosis until new habitat is encountered. To show departures from neutrality and recent dates for distinguish between these hypotheses, we used population colonization of the Central Pacific archipelagos, which is genetic methods to estimate larval dispersal among five consistent with frequent extinction and recolonization of South Pacific archipelagos in two amphidromous species of stream populations in this area. Similar results from other Neritid gastropod (Neritina canalis and Neripteron dilatatus). amphidromous species suggest that unstable freshwater Sequence data from mitochondrial cytochrome oxidase I habitats promote long-distance dispersal capabilities. (COI) revealed that neither species is genetically structured Heredity (2010) 104, 563–572; doi:10.1038/hdy.2009.138; throughout the Western Pacific, suggesting that their larvae published online 21 October 2009 Keywords: Neritina; Neripteron; South Pacific; larval dispersal; amphidromy; habitat instability Introduction estuaries, their planktotrophic larvae are released down- stream to the ocean, where marine salinities are required The life histories of marine and freshwater animals are for their successful development (Anger et al., 1990; generally very different: marine animals often have Diesel and Schuh, 1998; Crandall, 1999; Diele and Simith, planktonic larvae that are potentially dispersive (Thor- 2006). After metamorphosis and recruitment to river son, 1950), whereas freshwater animals typically develop mouths, juveniles migrate upstream to freshwater in benthic or brooded egg capsules, probably to reduce habitats (Schneider and Frost, 1986; Blanco and Scatena, dispersal and downstream loss from adult habitat 2005; Torres et al., 2006). (Holthuis, 1995; Bohonak and Jenkins, 2003). Notable Amphidromous species dominate the fish, decapod exceptions to this ontogenetic trend can be found in and gastropod stream fauna on tropical oceanic islands, diadromous species, which may reproduce in fresh most likely because they are the only lotic species water before recruiting to marine habitats (anadromy), capable of regularly colonizing these habitats (Resh and or reproduce in the ocean before recruiting to freshwater de Szalay, 1995; McDowall, 2004). However, although a habitats (catadromy). Amphidromy is a lesser-known community ecologist would view them as freshwater type of diadromy that has evolved independently in animals (for example, Bandel and Riedel, 1998; Smith several families of decapod crustaceans, gastropod et al., 2003), their population ecology may be more mollusks and teleost fishes (Myers, 1949; Holthuis, similar to that of a marine species, because of their 1995; McDowall, 2004). Although the adults of amphi- pelagically dispersing larvae. Relatively long pelagic dromous species live and reproduce in streams, rivers or larval durations (PLDs) have been estimated from laboratory cultures of amphidromous gastropod veligers Correspondence: Dr ED Crandall, Department of Biological Sciences, (40–98 days, Holthuis, 1995; Kano, 2006) and the otoliths Old Dominion University, Norfolk, VA 23529, USA. of amphidromous Galaxiid fishes and gobies (63–266 E-mail: [email protected] days, Radtke et al., 1988, 2001; Mcdowall et al., 1994; 1 Current address: Ecology and Evolutionary Biology, University of Hoareau et al., 2007b). These PLDs fall at or above the California Los Angeles, 621 Charles E Young Drive South, Los Angeles, CA 90095, USA high end of the range found in the planktotrophic larvae Received 16 November 2008; revised 18 August 2009; accepted 10 of marine invertebrates (7–293 days, Shanks et al., 2003) September 2009; published online 21 October 2009 and fish (B20–90 days, Brothers et al., 1983). High gene flow in amphidromous gastropods ED Crandall et al 564 Consistent with this high dispersal potential, Chaotic population dynamics have also been shown to genetic structure within high-island archipelagos is low promote the evolution of long-distance dispersal ability or non-existent in amphidromous Neritid and Neritiliid (Johnson and Gaines, 1990; Holt and Mcpeek, 1996). As snails (Hodges and Allendorf, 1998; Myers et al., 2000; the planktotrophic larvae of amphidromous species must Kano and Kase, 2004), as well as in Galaxiid and settle in a rare, unstable habitat, they could be selected Sicydiine fishes (Chubb et al., 1998; Waters et al., 2000; for the ability to delay metamorphosis and extend their Berrebi et al., 2005; Hoareau et al., 2007a), suggesting that planktonic life indefinitely (‘death before dishonor’ populations of amphidromous species are genetically hypothesis, Bishop et al., 2006, see Elkin and Marshall, structured at scales similar to fully marine species. In 2007 for a numerical model). Such a strategy could result contrast, fully lotic species are frequently genetically in extremely long-distance dispersal, limiting genetic structured within watersheds or even within reaches differentiation among archipelagos. (Bunn and Hughes, 1997; Marten et al., 2006). In this study, we assess mitochondrial genetic varia- Lotic habitats are rare in the South Pacific, occurring tion in two amphidromous snail species from the family only on volcanic islands that are tall enough to generate Neritidae (Gastropoda: Neritopsina). Neritina canalis their own adiabatic rainfall. Given the high levels of (Sowerby, 1825) and Neripteron dilatatus (Lesson, 1830) larval mortality and the effects of diffusion (Cowen et al., have planktotrophic larvae, as indicated by the 2000), it seems unlikely that significant numbers of larvae ‘D’-shaped initial region of their opercula (Kano, 2006) that drifted away from their natal archipelago would and probably share an amphidromous common ancestor be able to find suitable freshwater habitat for settlement. (Holthuis, 1995). Neritina canalis is found under stones in Therefore, local selection for traits that favor self- riffles within 1–2 km of the sea, and has a range that recruitment could be particularly strong for amphidro- extends from the Philippines to the Marquesas (Haynes, mous species (Sponaugle et al., 2002; Strathmann et al., 2001). Neripteron dilatatus is able to tolerate relatively 2002). Consistent with this prediction, Sorensen and high salinities (Liu and Resh, 1997), but has only been Hobson (2005) found that newly recruited amphidro- collected from rocky substrate in the estuaries of running mous gobies had stable isotope signatures that were streams ranging from the Philippines to the Society similar to inshore plankton rather than offshore plank- Islands (Pointier and Marquet, 1990; Haynes, 2001). If the ton, suggesting that larvae prefer to stay in coastal larvae of these species have developed behaviors for waters. Similar homing behaviors have been suggested retention in coastal waters, then we would expect to see for the larvae of amphidromous shrimp and snails genetic structure between or even within archipelagos. (Benstead et al., 2000; Haynes, 2000). Such larval Conversely, if the larvae are passively dispersed, but retention could result in limited realized dispersal and have adapted to extend their pelagic duration until they pronounced genetic structure among archipelagos. can recruit to freshwater habitat, then we would expect However, in addition to their rarity, riverine habitats to see little genetic structure across the South Pacific, on oceanic islands are inherently unstable. They are with relatively frequent long-distance dispersal and gene characterized by short overall lengths (generally o5 km), flow occurring in the direction of the prevailing currents. with small catchments, and extremely variable flows (Resh and de Szalay, 1995; Craig, 2003). Climactic fluctuations over the past several million years (Hope, Materials and methods 1996) and the rapid erosion and eventual subsidence of individual islands (Whittaker et al., 2008) ensure that Sampling and sequencing populations in oceanic island streams will be subject to We collected N. canalis (n ¼ 202) and N. dilatatus (n ¼ 151) local extinction and re-colonization over evolutionary from two or more islands in the West Pacific archipelagos timescales (Covich, 2006). These processes can be of Vanuatu Fiji, and Samoa, as well as from the Society expected to leave a molecular signature in the form of and Marquesan archipelagos in the Central