Longevity of Daphnia magna males and females
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- Pietrzak, B., Bednarska, A. & Grzesiuk, M. Hydrobiologia (2010) 643: 71. doi:10.1007/s10750-010-0138-6
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In many species, males are shorter-lived than females, and, mostly anecdotally, shorter lifespan was also attributed to Daphnia males. This does not necessarily stay in accordance with the biological roles of the sexes in Daphnia. Daphnia females maximize their fitness by maximizing the number of produced offspring, which incurs costs associated with quick attainment of large body size: metabolic costs of fast growth and increased risk of predation. In contrast, Daphnia males maximize fitness by maximizing the number of fertilized females, and seem to follow the strategy that enables them to maximize the lifetime female encounter rate, which should increase with lengthening lifespan. As arguments exist both in favour and against males living longer than females, we tested for differences in physiological lifespan of Daphnia magna males and females. Although maximum observed lifespan was always equal or longer in males than in females, no statistically significant differences were found. The results indicate that Daphnia males should not be considered short-lived anymore.
In many species, males and females apply contrasting strategies to maximize fitness, which results in conspicuous differences in morphology, behaviour and life history, including lifespan, of the individuals of different sexes (Hunt et al., 2004; Blanckenhorn, 2005; Maklakov et al., 2008). Among crustaceans, males have been shown to have shorter lifespan than females in amphipods (Moore, 1981) and krill, and this was observed both while males having similar (Siegel, 1987) or higher growth rate (Kawaguchi et al., 2007). Studies on social insects show, however, that under appropriate selection pressure the lifespan of males can be surprisingly long (Heinze & Schrempf, 2008).
As most Daphnia species are cyclic parthenogens and under favourable environmental conditions reproduce by amictic parthenogenesis, they form all-female clones, which often become the dominant component of lakes and ponds zooplankton communities. Daphnia switch to sexual reproduction when conditions deteriorate and only then males are produced and sexually receptive females appear in the population (Hebert, 1987). Fertilised eggs are encapsulated in a protective shell forming a structure called an ‘ephippium’ and are deposited during moulting as resting eggs, which can resume development when conditions recover (Hebert, 1987). Although sexual reproduction has important consequences for the long-term persistence of Daphnia populations, as it creates genetically diverse egg banks from which future populations can be established (De Meester, 1996; Grebelnyi, 1996), overwhelming majority of the studies have concentrated on the ecology of females, and investigations focusing on males fitness are rare.
A female maximizes fitness by maximizing the number of produced offspring, which incurs metabolic costs of fast growth and attainment of body size that enables assimilation of excess energy to lay numerous egg clutches. This, in turn, involves higher risk from visual predators, as it not only makes female more conspicuous, but also forces her to exploit the dangerous (albeit food-rich and warm) surface waters, where quick development may be reached.
Males, although genetically identical to their mothers and sisters (Hebert & Ward, 1972), play different biological role and thus apply different strategy to maximize their fitness. A male maximizes its fitness by maximizing the number of fertilized females, which involves encountering, contacting and copulating with as many receptive females of a different genotype as possible. This might incur less costs, as released from maximizing egg production, males grow more slowly, and reach smaller body size (MacArthur & Baillie, 1929a; Munro & White, 1975). They also stay deeper in the water column (Brewer, 1998; Spaak & Boersma, 2001; Mikulski et al., submitted), exhibiting behaviours which increase the potential of mating with females while reducing the risk of predation (Brewer, 1998). Brewer (1998) showed that Daphnia males swim faster than females, and on horizontal plane, orthogonal to the predominant swimming direction of females; similar ‘searching’ behaviours were also seen in other planktonic taxa (Kerfoot & Peterson, 1980; Watras, 1983). The need for the active seeking of a mate may explain the high metabolic demand, as males exhibit higher heart beat and CO2 production rate (MacArthur & Baillie, 1926; 1929b), and higher appendage beat frequency than females (Peñalva-Arana et al., 2007). At the same time, males were shown to be more temperature-sensitive (MacArthur & Baillie, 1929a), but less sensitive to the presence of stressors such as cyanobacteria (Lürling & Beekman, 2006), high concentrations of dissolved humic substances (Euent et al., 2008) and chemical compounds such as potassium dichromate or chlorophenols (Ikuno et al., 2008) (but see Breukelman, 1932).
Low investments in early growth (Metcalfe & Monaghan, 2001), staying in safe habitat, free of predation threat (Kirkwood & Austad, 2000), high swimming performance (Reznick et al., 2004), and stress resistance (Jazwinski, 1996), have all been associated with longer physiological lifespan. Also, long life at minimum risk supports the biological role of the male—maximizing the number of fertilized females. Moreover, although small body size and high metabolic rate have traditionally been associated with shorter physiological lifespan (Sohal et al. 2002), smaller individuals with higher rates of metabolism have also been shown to live longer than their slower and larger conspecifics (Speakman, 2005). As there are reasons both in favour and against males being longer lived than females, the objective of this article is to test for possible differences in physiological lifespan between Daphnia magna males and females. A life-table experiment was performed to test this hypothesis and its results are discussed.
The experiment was performed in filtered lake water at 20°C under summer photoperiod (16L:8D) using three clones (referred to as: D2, B8I and B8II) of Daphnia magna hatched from ephippia collected from sediments of Binnensee (northern Germany). Experimental animals within a clone were cultured from a single female under the above conditions, second clutch always taken for further culture. Male production was induced by crowding (50 ind. l−1). Neonates born within 12 h were separated from the mothers and their sex was determined within 2–3 days. 30 females from each clone were randomly assigned to one of 6 replicate vessels, each vessel with five individuals at the start of experiment. 30 males from each clone were similarly assigned to another set of six replicate vessels. Population density in experimental vessels was kept constant at 1 individual per 80 ml medium by adjusting the amount of medium according to the number of individuals alive. The animals were fed daily with suspension of green alga, Scenedesmus obliquus, given in concentration equal to 1 mg Corg l−1. Every second day the water was changed, offspring was removed and the surviving individuals were counted. The experiment lasted until the natural death of all individuals.
Prior to analysis, data were tested for normality with Shapiro–Wilk test and, as ANOVA assumptions were not met, analyzed by non parametric tests. Significant differences were established at P < 0.05. As there were no between-replicate differences in lifespan within groups, data were pooled. The Wilcoxon (Gehan) test was used to test the hypothesis that the survival functions between males and females within a clone were equal.
Results of two-sample Gehan-Wilcoxon survival tests for male and female lifespans within clones
Daphnia males, as smaller than females of the same age, and appearing in the population only temporarily, have been anecdotally considered to be short lived, data, however, are scarce, and if available, from single clone studies only. Some early authors (MacArthur & Baillie, 1929a) indeed showed that males lived shorter than females. These authors have also found that male lifespan is more sensitive to temperature (MacArthur & Baillie, 1929a). More recently, Euent et al. (2008) also showed shorter lifespan of males, which was though increased in a hormetic manner upon exposure to humic substances (increased lifespan under low stress levels). The short lifespan of males stays in accordance with the rate of living hypothesis, as Daphnia males are smaller and have higher metabolic rate (MacArthur & Baillie, 1929b).
However, males maximize fitness by maximizing the number of fertilized females, and seem to follow the strategy that enables them to maximize the lifetime female encounter rate, that is ‘keep fit’ and ‘stay out of danger’, exhibiting high swimming performance (Brewer, 1998) and staying in deeper strata where fish predation risk and rate of living are low (Mikulski et al., submitted). We therefore hypothesized that the physiological lifespan of Daphnia magna males might be longer than that of females. As we did not detect any significant differences in physiological lifespan between males and females, our results indicate that Daphnia males should not be considered short-lived anymore.
Heritable physiological changes leading to longevity might have, according to antagonistic pleiotropy theory, negative consequences to early fecundity (Williams, 1957), which would be a particularly negative trait in, genetically identical to males, Daphnia females. Thus, Daphnia males could achieve the hypothesized longer lifespan behaviourally, by migrating to deeper strata and staying through their lives at or below the thermocline (Brewer, 1998), where not only lower temperature but also lower food supply would influence their lifespan. The temperature was kept constant at 20°C in our experiment; however, it is very plausible, that given the possibility to choose the habitat temperature, males would modulate their realized lifespan by staying in cold water. Although this is very likely occurring in nature, the aim of this study was to track differences in physiological lifespan between sexes, and such are not excluded by our results. Indeed, physiological differences are expected in light of the broad scope of phenotypic plasticity of Daphnia genotype, which has been shown both on individual (Dodson, 1989; Stibor, 1992) and molecular level (e.g. heat shock protein expression, Pijanowska & Kloc, 2004). A more detailed study using more clones and/or more individuals within treatments can yield significant differences. Moreover, as MacArthur & Baillie (1929a) stressed differences in lifespan sensitivity to temperature of males and females, choosing different habitat temperatures, experimental thermic conditions may influence the results.
Another interesting point to consider would be the food concentration and population density. Daphnia longevity is strongly influenced by food levels (Ingle et al., 1937; Martínez-Jerónimo et al., 1994; Muńoz-Mejía & Martínez-Jerónimo, 2007) and can be twofold extended by dietary restriction (Pietrzak et al., 2010), and in an anostracan crustacean such lifespan extension was shown to be more pronounced in males than in females (Anaya-Soto et al., 2003). As males and females differ in filtration rates (personal observation), which is probably a consequence of body size, they may also differ in assimilation rates, and thus food ad libitum and ‘restriction’ levels. If so, it shall in future be considered, that what is ad libitum to a male, may be dietary restriction to a female (but Peñalva-Arana et al. (2007) hypothesize conversely). In our experiment, both sexes were given equal amounts food set at a concentration well above the incipient limiting level (Bohrer & Lampert, 1988). However, were the food conditions adjusted to sex-specific needs, that is, supposedly, were males given less food, longer lifespan of males would be expected. Differences in the food uptake between males and females are currently under study in our lab. Population density is mentioned here, as it determines amounts of food available per capita, and as rearing animals individually may reveal differences obscured by the fact, observed in other species, that male–male interactions reduce lifespan (Gems & Riddle, 2000).
Finally, as the induction of male production and sexual eggs production are independently controlled (Hobaek & Larsson, 1990; Kleiven et al., 1992), this uncoupling in time of appearance of males and receptive females within a clone may serve to avoid selfing (De Meester & Vanoverbeke, 1999; Berg et al., 2001). Under conditions of dynamic population structure and seasonal succession of clones, long-lived males would gain advantage of higher probability of encountering females of different genotypes. While our study did not show differences in physiological lifespan between males and females, future direction of the research will be to show whether males attain longer lifespan behaviourally by staying in colder and poorer in food resources deeper strata.
This study sheds some new light to Daphnia males and females longevity, as parts of their life histories subject to different selection pressures, and although many questions remain, it opens the discussion on the so far ignored role of males in maximizing the clonal fitness.
We want to thank the two anonymous reviewers and Joanna Pijanowska for valuable comments on the manuscript. This study was supported by Polish Ministry of Science and Higher Education grants N304 005 32/0647 and N N304 094135.