Transgenerational effects of parental nutritional status on offspring development time, survival, fecundity, and sensitivity to zinc in Chironomus tepperi midges

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Highlights

  • Changes in life history traits and metal resistance in offspring were examined.

  • Parental nutritional status induced plastic changes through non-genetic inheritance.

  • Lower nutritional status of parents caused more rapid development in offspring.

  • The fecundity endpoint seems to be more affected by parental nutritional status.

  • The transgenerational effects observed were not specifically for sensitivity to Zn.

Abstract

Environmental stimuli can induce plastic changes in life history traits, and stimuli experienced by parents can be transmitted to the next generation (“transgenerational”) through the inheritance of factors unrelated to changes in DNA sequences. Transgenerational effects are common in species living in habitats subjected to recurrent stressful events, such as fluctuating resource availability. In a previous study, the nutritional status of the midge Chironomus tepperi has been reported to influence life history traits of the offspring. In this study we investigated whether they also alter sensitivity of offspring to zinc. Offspring of parents reared under low food conditions had a shorter development time and lower reproductive output compared to offspring of parents raised under excess food. While zinc exposure decreased the survival of offspring generally, the interaction between parental food level and zinc exposure did not influence the relative sensitivity of offspring toward zinc. Parental nutritional stress therefore triggered transgenerational effects, potentially acting as confounding factors in ecotoxicological studies, but they did not directly affect the susceptibility of offspring to zinc.

Introduction

The expression and evolution of life-history traits of an individual are a product of the interactions among its genotype, the environment in which it is raised, and parental traits (Bernardo, 1996, Mousseau and Fox, 1998, Rossiter, 1991). Environmental stimuli can induce plastic variations in the life history traits of an organism without corresponding alterations in the genome. Such variations experienced by the parents can be transmitted to the offspring through the inheritance of factors other than alterations in DNA sequences (non-genetic inheritance or transgenerational effects) (Bonduriansky and Day, 2009, Giesel, 1988).

Transgenerational effects combine a diversity of phenomena such as epigenetic modification of gene expression, hormonal induction, transmission of immunological factors produced as a result of exposure to pathogens, behavioural inheritance and ecological inheritance of modified environments (Jablonka et al., 1998, Mousseau and Fox, 1998, West-Eberhard, 2003). Parental effects have been shown to influence life history traits and create fitness variation among individuals in a population (Harrison et al., 2011, Mousseau and Fox, 1998), thereby potentially influencing the structure of a community. Such effects are predominantly transient, dependent on the environmental conditions, and specific to species (Agrawal et al., 1999).

Transgenerational effects occur frequently among species living in habitats subjected to rapid changes or recurrent stressful events (Zehnder and Hunter, 2007). In fluctuating environmental conditions, such effects can become critical if they confer to the offspring the ability to rapidly adjust to changing conditions, thereby increasing fitness regardless of genetic constraints. Moderate stress can lead to the appearance of stress tolerance or avoidance, as well as the development of novel characteristics in the offspring generation (see Badyaev, 2005, Hoffmann and Parsons, 1991). Offspring of stressed parents born with a favourable phenotype already expressed do not need a lag phase to stimulate the response. For example, in Daphnia cucullata, the offspring of parents exposed to predation are born with a maternally induced defence (maximally large helmet), while short-headed offspring of non-exposed parents are vulnerable to predation (Agrawal et al., 1999). If a stressor is different from that experienced by the parents, a novel and potentially suitable phenotype may be more likely expressed in offspring of stressed parents as phenotypic variability will be increased in this offspring generation (Badyaev, 2005, Mousseau and Fox, 1998). Transgenerational effects may therefore be critical in surviving unfavourable or unpredictable environmental conditions (Jablonka and Raz, 2009, Mousseau and Dingle, 1991, Plautz et al., 2013a).

In insects, alterations in the accumulation of metabolic resources can affect offspring fitness. For example, the quality of parental diet in the Indian meal moth (Plodia interpuctella) and in the gypsy moths (Lymantria dispar) influences the development time of the offspring, with a high quality diet leading to a fast development time of the offspring (Rossiter, 1991, Triggs and Knell, 2012). In addition, a reduction in nutrition can influence offspring fitness. A mild starvation (moderate stress) may increase stress resistance to heat in offspring of Drosophila (Bubli et al., 1998), while Daphnia reared under poor conditions can produce offspring more resistant to bacterial pathogen than those raised in favourable conditions (Mitchell and Read, 2005). Nutrition constraints also have been reported to be an important driver of epigenetic modifications in rats (Lillycrop et al., 2005).

Transgenerational effects have received considerable attention in ecological and evolutionary fields but less so in ecotoxicology (Pieters and Liess, 2006), although they have been considered in two recent reviews (Head et al., 2012, Vandegehuchte and Janssen, 2011). Although fluctuations in resource availability are a recurrent scenario in freshwater environments, few studies have investigated the effects of parental diet on the offspring tolerance to toxicants (Buikema et al., 1980, McCauley et al., 1990). Most studies have focussed on Daphnia magna (Enserink et al., 1993, Enserink et al., 1990, Pieters and Liess, 2006) where variation in food provisioning affects fecundity: mothers reared on diets of poor quality and quantity produce small broods with large neonates, whereas mothers raised on abundant or high quality food produce large broods of small neonates (Cowgill, 1987, Smith, 1963). In turn the small neonates of well-fed mothers may be more sensitive than large neonates from small broods to some pollutants (Baird et al., 1989, Enserink et al., 1990, Pieters and Liess, 2006). Such findings raise the issue of whether transgenerational effects need to be integrated in ecotoxicological tests designed to assess the impact of pollutants on aquatic organisms (Baird et al., 1989, Cox et al., 1992).

The potential effect of parental nutritional status on offspring sensitivity in Chironomus species has not been considered in detail, although these species are widely used in ecotoxicological testing. Chironomus species have a high reproductive rate when food resources are abundant and low when food is scarce (among others Ristola, 1995, Sibley et al., 1997). Offspring growth rate is thought to be independent of maternal mass and growth rate (Liber et al., 1996). However, Townsend et al. (2012) found that in Chironomus tepperi offspring were influenced by the nutritional status of the parents.

The present study considers the effects of parental diet of C. tepperi on the life history and metal sensitivity of offspring. We focus on zinc because this metal is extensively used in manufacturing and industrial processes (e.g. paints, electroplating industry, pesticides, mining) and is also found in urban and residential areas (e.g. from shedding of car tyres, galvanised roofs, wood preservative leaching) (ATSDR, 1995, Councell et al., 2004). Zinc enters the aquatic environment through stormwater runoff from industrial and urban areas (Callender and Rice, 2000) and accumulates to high concentrations in the environment (Cain et al., 2013, Hare, 1992), although the fate, bioavailability and toxicity of zinc are strongly influenced by factors such as pH (Krantzberg and Stokes, 1988), salinity, temperature, hardness of the water (Bryan, 1971, McLusky et al., 1986) and oxygen (Burton et al., 2006).

We consider parental generations reared under different feeding regimes whereas the offspring were assessed in a common environment (standard feeding regime). Offspring survival, development time, fecundity, and sensitivity toward zinc exposure were monitored to test the hypothesis that parental exposure to stress might provide an advantage to offspring when exposed to zinc.

Section snippets

Experimental overview

This study is divided in two parts (Fig. 1). The first experiment, named “Parental effects”, was designed to verify whether transgenerational effects are inducible in C. tepperi by varying nutritional status. This was achieved by exposing the parents to different feeding regimes and raising their offspring in an optimal standard regime. Differences observed in the chosen life history traits were attributable only to a parental influence (Fig. 1a).

The experimental protocols were adapted from

Offspring survival and development time

Offspring survival (scored as successful emergence) reached 70 percent in all treatments; although offspring of low-food parents showed a slightly higher survival (high-food: x¯=14.75, SD=0.5; standard-food: x¯=14.5, SD=2.88; low-food: x¯=17, SD=2.16), the difference among the treatments was not significant (F2, 9=1.717, p=0.234). In contrast, an effect on development time was evident. Levene’s test indicated that the homogeneity of variances was violated (F2, 9=5.422, p=0.028), and hence

Discussion

According to our results, nutritional stress in C. tepperi can trigger transgenerational responses. Offspring whose parents were reared under low-food conditions had a shorter larval development time than offspring whose parents were raised under high-food conditions. Survival was not significantly different between treatments although a trend was present in both experiments, with offspring of low-food parents having a higher survival rate. The opposite response was visible in the reproductive

Acknowledgments

We thank Kallie Townsend for insight and useful comments on the manuscript. Funding for this research was provided by Melbourne Water Corporation, The Victorian Department of Business and Innovation through support of the Centre for Aquatic Pollution Identification and Management, and the Australian Research Council through their Fellowship scheme.

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