Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology
Effects of maternal stress on egg characteristics in a cooperatively breeding fish
Introduction
Stress, resulting from sudden perturbations (acute) or from constant challenges (chronic) in the environment, induces a suite of important physiological and behavioural responses. Natural selection has shaped stress responses to enhance an organism's ability to cope with the stressor and to eventually regain homeostasis (Chrousos, 1998, Charmandari et al., 2005). A key component of the physiological stress response is the mobilization of glucocorticoid (GC) stress hormones (cortisol or corticosterone) via activation of the hypothalamic-pituitary-adrenal (HPA, in tetrapods; in fish the HPI or hypothalamic-pituitary-interrenal) axis. The ability to mount an appropriate stress response is generally considered beneficial. However, a prolonged elevation of GCs in response to long-term exposure to stressors can have detrimental effects on an individual, including reductions in growth and immune function, and the suppression of reproduction (Chrousos, 1998, Wendelaar Bonga, 1997, Charmandari et al., 2005, Schreck, 2010). Stressful conditions experienced early in life (or in utero) may have profound impacts later in life (Contreras-Sanchez et al., 1998, Rondó et al., 2003, Hayward and Wingfield, 2004, Ostrand et al., 2004, Sloman, 2010). In this study, we used a cooperatively breeding fish species to explore whether stress experienced by breeding females projects onto the next generation. We examined the effects of chronic maternal stress (induced by repeated exposure to an acute stressor) on female reproductive rates, fecundity, and egg characteristics.
To our knowledge, the potential fitness costs of maternal stress have not yet been experimentally manipulated in cooperatively breeding species. Cooperative breeders are group-living species, in which subordinate group-members forgo reproduction to help raise the offspring of dominant individuals. We predicted that the effects of maternal stress on offspring number and quality would be exaggerated in social cooperative breeders due to the energy requirements and challenge of maintaining dominance over subordinates in the social group (see Goymann and Wingfield 2004). To date, the impact on reproductive success of maternal stress during gestation has been studied in several species that are not cooperative breeders. For example, maternal stress results in lowered birth-weight in human, Homo sapiens, infants (Rondó et al. 2003), slower juvenile growth rates in Japanese quail (Coturnix coturnix japonica, Hayward and Wingfield 2004), smaller egg clutches in moor frogs (Rana arvalis, Räsänen et al., 2005), and smaller eggs and young in rainbow trout (Oncorhynchus mykiss, Campbell et al. 1992; Contreras-Sánchez et al. 1998).
To address the impact of maternal stress on reproductive fitness in a cooperative breeder, we used the cichlid fish, Neolamprologus pulcher, endemic to Lake Tanganyika, Zambia. N. pulcher live in highly social groups organized into linear dominance hierarchies based on size, with a breeding male and female pair at the top of the hierarchy and 1-20 subordinate helpers (Taborsky and Limberger, 1981, Balshine et al., 2001, Heg et al., 2005). The dominant breeders remain in their position for 3-12 months (Stiver et al. 2004) and subordinates rarely breed in the wild but can eventually gain dominance and breeding status, via inheritance or take-over (Fitzpatrick et al., 2008, Stiver et al., 2009). N. pulcher groups live in communally defended rocky territories clustered together into subpopulations at 3-45 metres depth (Stiver et al. 2008). In these territories, female breeders may be exposed to a number of potential environmental and social stressors. First, breeders often experience elevated predation pressure and frequently defend their young against predators (Balshine et al. 2001). Second, individuals constantly need to vigorously defend their territories against encroaching, neighbouring conspecifics as well as heterospecific space competitors (Desjardins et al. 2008). Third, dominant breeders must police subordinates to control their reproduction (Goymann and Wingfield, 2004, Fitzpatrick et al., 2008). Exposure to such stressors has the potential to repeatedly raise GC levels and therefore could have fitness implications for both breeding females and their offspring.
We made a series of predictions for the effects of maternal repeated stress on reproductive fitness in N. pulcher based on findings in the literature. One, we predicted that stressed breeder females would take longer to reproduce. In rainbow trout, both chronic and acute stress caused delays in ovulation and spawning (Campbell et al., 1992, Contreras-Sanchez et al., 1998). Two, we predicted that stressed fish would lay fewer, smaller eggs, as chronic stress was found to reduce egg mass in rainbow trout (Campbell et al. 1992; reviewed in Schreck et al. 2001). Three, we predicted that cortisol levels would be higher in the eggs of stressed compared to those of unstressed (control) females. Similar findings of maternal transfer of GCs have been observed in egg yolk of Japanese quail (Hayward and Wingfield 2004) and in the eggs of coho salmon, Oncorhynchus kisutch (Stratholt et al. 1997). A final prediction stems from the novel aspect of our study. We predicted that the presence of helpers would increase the stress experienced by breeder females and therefore that females with more helpers would exhibit a heightened response to an experimental stressor. This notion is supported by work in which female damselfish (Pomacentrus amboinensis, a coral-dwelling social fish), in environments with multiple conspecifics exhibited higher cortisol levels and consequently hatched smaller juveniles than those that were allowed to breed in isolation (McCormick 2006). Goymann and Wingfield (2004) predicted that there would be greater physiological stress (termed allostatic load) for dominant individuals in species where acquiring and maintaining dominance is difficult. In N. pulcher, few individuals manage to attain a breeding position and individuals that do so must regularly assert their dominance to maintain their position (see Mileva et al. 2009 for a full allostatic load calculation for N. pulcher). Thus we predicted that under normal control conditions, breeding females with helpers or with many helpers would lay eggs containing higher cortisol levels than females without helpers or with few helpers. We also aimed to investigate the effects of helper presence on egg size in stressed females.
Section snippets
Fish husbandry and housing
All fish (Neolamprologus pulcher, Cichlidae) used in this experiment were held at McMaster University, Hamilton, Ontario, Canada. They were either descendants of wild-caught breeding pairs captured in 2002, or were wild-caught breeding pairs from early 2008, captured at the southern tip of Lake Tanganyika. Twenty stable social groups, ones in which spawning had occurred prior to the beginning of the experiment, were chosen for use in this experiment. Each social group was housed in a 189 L tank
Females
Prior to exposure to stress, control females and females in the stress treatment did not differ in body mass, standard length or body condition (body mass: Mann Whitney U test, U = 0.61, p = 0.44; standard length: t-test, t15 = 1.41, p = 0.18, body condition, t15 = -1.18, p = 0.26; Table 1). Over the course of the experiment (controlling for differences in spawning interval, see above), females in the stressed treatment gained less mass (some even lost mass) compared to control breeder females (ANOVA,
Discussion
This study provides evidence that N. pulcher breeder females repeatedly exposed to acute stress experienced a decline in maternal fitness and is suggestive of possible offspring fitness costs. Stressed N. pulcher females experienced longer intervals between spawning events, and laid fewer eggs of smaller mass than control females. The results suggest that not only is maternal fitness influenced by repeated acute stress, but that maternal stress may have repercussions for offspring fitness owing
Acknowledgements
We would like to thank Chris M. Wood for allowing us to use his facilities, Linda Diao, and especially Derek Alsop for help with cortisol analyses. We would also like to thank Julie Marentette and Susan Marsh-Rollo for help with egg counting and cortisol extraction, respectively. This research was funded by Natural Sciences and Engineering Research Council of Canada Discovery, and Research Tools and Instruments grants to SB and KMG, as well as by the Ontario Innovation Trust and Canadian
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