Oecologia (2001) 129:220–227 DOI 10.1007/s004420100712
C. Barata · D. J. Baird · A. M. V. M. Soares
Phenotypic plasticity in Daphnia magna Straus: variable maturation instar as an adaptive response to predation pressure Received: 16 November 2000 / Accepted: 4 April 2001 / Published online: 31 May 2001 © Springer-Verlag 2001
Abstract Life history responses of four Daphnia magna clones at two food levels were studied to assess the importance of maturation instar on the plasticity of fitness responses under simulated mortality regimes. Females of the clones studied could vary offspring size with consequent effects on their maturation time. Significant genetic variability in life history and fitness responses, measured as the intrinsic rate of population increase, within and across food levels was observed, but most of this variation could be attributed to maturation instar differences among clones within and across environments. In the laboratory, without extrinsic mortality, females maturing earlier always had higher fitness than those maturing later, indicating a clear fitness cost of delaying maturity. Nevertheless using a model, we showed that the observed maturation instar effects on life history responses can lead to differences in fitness under different sizeselective predation regimes, such that females with delayed maturity have higher fitness under invertebrate predation while females maturing earlier have higher fitness under fish predation regimes. These results suggest that intraclonal variation in offspring size and hence in the number of maturation instars can be an adaptation to living in habitats subject to temporal fluctuations in fish and invertebrate predation pressure. Keywords Genetic variability · Offspring size · Mortality · Predation
C. Barata (✉) · A.M.V.M. Soares Departamento de Biologia, Universidade de Aveiro, Campus de Santiago, 3810-193 Aveiro, Portugal e-mail:
[email protected] Tel.: +44-1786-467874, Fax: +44-1786-472133 D.J. Baird Institute of Aquaculture, University of Stirling, Stirling, FK9 4LA, UK C. Barata Institute of Aquaculture, University of Stirling, Stirling FK9 4LA, UK,
Introduction Phenotypic plasticity within populations has primarily been studied in the context of genetic adaptations to environmental fluctuations (Via et al. 1995; DeWitt et al. 1998; Scheiner and Callahan 1999 among others). However knowledge and understanding of the phenotypic mechanisms generating plasticity are limited (Brakefield et al. 1996). Assessing these mechanisms and their fitness implications is essential for understanding their evolutionary significance (Bernardo 1993). Here we attempt to explain one of the possible mechanisms behind genetic variability in phenotypic plasticity in life history traits in Daphnia magna and its potential fitness consequences. One of the most important features of Daphnia life histories is the ability to vary the number of developmental instars required for females to reach maturity (hereafter referred to as maturation instars). According to the maturation size threshold hypothesis of Ebert (1991, 1992, 1994, 1997) and other studies (McKee and Ebert 1996; Barata and Baird 1998), variability in the number of maturation instars depends on genetic and environmental variation in the threshold size for initiation of maturation, offspring size and juvenile growth rates. Thus, it is not surprising to find high levels of variability in the number of maturation instars among genotypes within environments (genetic variability), among genotypes across environments (genetic variation in plasticity: Ebert 1991, 1994; Barata and Baird 1998) or even within a given genotype and environment (intraclonal variability: Ebert 1991; Barata and Baird 1998). Ebert (1991, 1992, 1994) and Barata and Baird (1998) showed that variation in offspring size, by determining the number of developmental instars to maturity in D. magna, was one of the major mechanisms generating phenotypic plasticity in age, body size and clutch size at maturity. Indeed the studies mentioned above found that females which were born smaller or developed under low food levels required more instars to mature than females which were born larger or which developed at
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high food levels. Delaying reproduction by only a single instar will result in increased age, body length and clutch size at maturity. Moreover, within a particular maturation instar group, body length and clutch size at maturity will increase with offspring size. Although life history and fitness consequences of varying offspring size and the number of maturation instars have been studied (Tessier and Consolatti 1989; Ebert 1991, 1992, 1994; Boersma 1997; Barata and Baird 1998), life history traits calculated in the above-mentioned studies did not represent realistic fitness scenarios, since natural mortality rates were not included (Roff 1992). Several studies have convincingly demonstrated that predation has a major impact in freshwater communities in general (Carpenter and Kitchell 1993) and, in particular, on the genetic composition of Daphnia species (De Meester 1996). Predators can structure zooplankton populations directly through size-selective predation, with fish usually preferring larger individuals and a variety of invertebrate predators selecting smaller-sized individuals. As a consequence, given the importance of predation, life history patterns of Daphnia populations are expected to show adaptations to the predation pressure in their local habitat (Boersma et al. 1999). Our aim was to study the importance of maturation instar on the plasticity of fitness responses under simulated mortality regimes. We hypothesised that intraclonal variation in offspring size and hence in the number of maturation instars is an adaptation to living in habitats which are subject to temporal fluctuations of fish and invertebrate predation pressure. Because fish predation selects against larger individuals, maturing earlier at smaller size increases chances for successful reproduction. Alternatively, when fish are absent, invertebrate predators tend to increase in abundance, and since invertebrate predators select against smaller individuals, being born larger is advantageous, even though this may lead to delays in maturation (Brooks and Dodson 1965; Post and McQueen 1987). This hypothesis was tested by studying the effects of the number of maturation instars invested to maturity on genetic variation in phenotypic plasticity of life history responses of four D. magna clones across two food environments (Barata and Baird 1998). Life history responses included age at first reproduction, body size, offspring size, size of first clutches and the intrinsic rate of population increase, r (which is often used as a synonym for fitness: Roff 1992). To assess the fitness consequences of being small and maturing earlier or being large and maturing later, we ran simulated experiments with two mortality regimes representing fish and invertebrate predation.
Materials and methods Experimental animals The animals used in this study were obtained from four genetically distinct laboratory clones of D. magna designated F, C, A and S-1 that originated from geographically separate populations (Baird et al. 1991; Barata and Baird 1998).
Experimental design A two-way ANOVA design was used for the experiments, consisting of four clones exposed to two food concentrations, 0.4 and 1.8 mg C l–1 of Chlorella vulgaris Beijerinck (Barata and Baird 1998), henceforth referred to as low and high food concentrations, respectively. To minimise maternal effects (Lynch and Ennis 1983), all experimental animals originated from third-brood females acclimated to each food concentration for more than five generations. For each particular clone and food combination, =11 neonates
