Sex-related differential mortality of a marine copepod exposed to a toxic dinoflagellate

In this study we hypothesized that the sexes of the copepod Acartia hudsonica experience different mortalities when exposed to the toxic dinoflagellate Alexandrium fundyense. In laboratory experiments, we manipulated toxin dose and measured sex-specific mortality. We also used a split-family design to determine whether there were genetic influences on sex determination, and therefore on sex ratio. When the dose of the toxic alga was high (25% of diet by carbon content), population mortality was high, and the fraction of males surviving to adulthood was low (20–30% of the adult population). No such effect was observed when A. fundyense comprised only 10% of the diet. Adult male copepods were also more susceptible to the toxic alga, though prior selection for resistance to toxins also had an effect on mortality. No genetic variation for sex ratio was detected in the split-family experiment. Males of A. hudsonica are more sensitive to the toxins of A. fundyense than are females. Resistance may be sex-linked, and copepod populations exposed to a bloom of toxic Alexandrium sp. may experience shifts in sex ratios away from males and toward females. Differential mortality and skewed sex ratios are feedback mechanisms potentially affecting both the population dynamics of grazers and the development of toxic algal blooms. Under most circumstances a population of sexually reproducing organisms ought to have an equal sex ratio, one male for every female. If, for some reason, the sex ratio deviates from 1 : 1, frequency-dependent selection should restore the ratio to 1 : 1 (Fisher 1930). Nevertheless, skewed sex ratios are known to occur. For example, when mothers control the sex ratio of a brood and fitness differs between sexes in the brood, the sex ratio of the offspring should be skewed toward the sex that will provide the mother with the highest relative fitness gains. In such a case, the sex ratio is considered adaptive (Charnov 1982). However, not all skewed sex ratios should be considered adaptive; some may simply be the result of transient shifts away from a normal 1 : 1 ratio (Charnov 1982). Sex ratios that deviate from one male for every female are often observed in populations of free-living pelagic copepods. Several reasons have been suggested for these observations, including sex change (Fleminger 1985; Lee et al. 2003), differential development rates or mortality rates (Conover 1965; Lee and McAlice 1979), and environmental sex determination (ESD) influenced by nutrition (Irigoien et al. 2000). Most often females are found to be favored in copepod populations. Sex ratios skewed toward females may have either positive or negative consequences for these populations. For instance, if the sex ratio at birth is biased toward females, then constraints on permissible egg mortality are relaxed (Dam and Tang 2001). Also, if mating encounters and subsequent fertilization are not limited, then a preponderance of females will enhance population growth rate. On the other hand, skewed sex ratios may have negative consequences. For example, copepods are obligatorily sexual, and fertilization is internal. Therefore, finding a mate and copulating is necessary for mating success and production of viable eggs. Any factor that skews sex ratios toward females and away from males might adversely affect population growth rate through mating limitation. Kiørboe (2007) found that at least one species of copepod could encounter mating limitation, a situation in which male copepods fertilized only one third of females. He suggested that unmated females are the source of nonviable eggs often observed in the field. In another study, Rey-Rassat et al. (2004) attributed periods of low population egg production in Calanus helgolandicus to unfertilized females. In order to understand the ramifications of skewed sex ratios, we must know the inherent sex-determining mechanism of organisms (Bull 1983). Sex determination among harpacticoid copepods has been studied (Voordouw and Anholt 2002a,b; Voordouw et al. 2005), but such studies among other groups are fewer. In the calanoid genus Acartia, a chromosomal (genotypic) mechanism of sex determination has been reported. Males are heterogametic (XO) and females homogametic (XX) (Goswami and Goswami 1974; Lecher et al. 1995). Such a mechanism of sex determination is predicted to yield a sex ratio at fertilization of 1 : 1 (Bull 1983). Therefore, species in the genus Acartia sp. are promising models to understand changes in sex ratio that occur after fertilization. We have been using the calanoid copepod Acartia hudsonica as a model organism to investigate copepod 1 Present address: Yale University, Osbourne Memorial Laboratories, 165 Prospect St., New Haven, Connecticut 06511. Acknowledgments We wish to thank David Kulis and Don Anderson of the Woods Hole Oceanographic Institution for analyzing toxins. We also wish to thank anonymous reviewers for commenting on the manuscript. The research and its publication were supported by the Ecology and Oceanography of Harmful Algal Blooms (ECOHAB) program through grants from National Oceanic and Atmospheric Administration (NA160P1458, NA06NOS4780249) and the Environmental Protection Agency (EPA) (RD-8317060) and by National Science Foundation grant OCE-0648126. This research does not necessarily reflect the views of the EPA, and no endorsement should be inferred. Limnol. Oceanogr., 53(6), 2008, 2627–2635 E 2008, by the American Society of Limnology and Oceanography, Inc.