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Adaptive significance of transgenerational plasticity in the wild

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The world´s oceans are warming at unprecedented rates (IPCC 2014), and organisms need to respond to these fast changing environments. Response mechanisms include migration (shifting distributions), rapid evolution (genetic tracking) and/or adaptive phenotypic plasticity (reviewed in Munday et al. 2013). Plasticity can occur both within a generation (individual genotype responds to environment) and across generations (transgenerational plasticity or TGP). For TGP, the environment that parents experience influences offspring plasticity, manifest as a parent environment by offspring environment interaction (Mousseau & Fox 1998). When parent and offspring environments match, TGP is likely to play an important role in coping with rapid climate change (Engqvist & Reinhold 2016) because it is a fast, phenotypic response that is inherited across generations, potentially buying time for slower genetic change to catch up in the longer term (Chevin et al. 2010; Bonduriansky et al. 2012). The number of studies documenting TGP in response to simulated climate change scenarios has exploded over the past few years (reviewed in Donelson et al. 2018). In many cases, acclimation of parents to rapidly changing environmental conditions resulted in compensation of offspring traits to otherwise negative effects. For example, TGP in response to climate warming, changes to salinity and ocean acidification was shown in numerous taxa spanning the tree of life (Salinas et al. 2013), with benefits for offspring traits such as improved survival, development, growth, fecundity and metabolism (Donelson et al. 2018). What is missing from the current TGP-climate change literature, however, are studies examining the adaptive significance of TGP for direct measures of fitness, specifically, the role of TGP in mate choice and reproductive success (but see Donelson et al. 2016).

Reproductive success is the ultimate measure of fitness, and can be defined as the passing of genes onto the next generation, such that those genes will then pass to further generations (Clutton-Brock 1988). Since reproductive success is not solely determined by the number of offspring produced, but also the probable reproductive success of those offspring, mate choice plays an important part in this success (Batesen 1983). Mate choice is the process that occurs whenever the effects of traits expressed in one sex lead to non-random mating with members of the opposite sex (Kokko et al. 2003). The topic of mate choice is vast (reviewed in Edward 2015), and a comprehensive treatment of this broad research area is beyond the scope of the current study. Briefly, in resource-based mating systems, the choosing sex, typically the female, selects partners based on direct benefits (i.e. resources such as food, shelter, parental care or protection). In nonresource-based systems, genetic components such as ‘good’ or ‘compatible’ genes often constitute an important factor mediating mate choice (Kokko et al. 2003). Recently, theoretical models have drawn attention to how non-genetic inheritance mechanisms such as epigenetic marks and TGP can also lead to adaptive (or non-adaptive) traits in offspring that influence sexual selection and mate choice (Bonduriansky & Day 2013). Both the expression of sexual traits (e.g. body size, ornamentation, condition) as well as mating preferences for these traits can be altered by parental effects (Qvarnström & Price 2001). However, empirical studies explicitly demonstrating the interaction between parental environment, offspring environment and offspring mate choice are scarce (but see examples of sexual imprinting; Pfennig & Servedio 2013; Head et al. 2016).

Mate choice is expected to select for traits that reliably indicate mate quality and/or compatibility (Kokko et al. 2003), but environments change in space and time, and cues that are indicative of mate quality in one environment may represent sub-optimal or maladaptive cues under changed conditions. In the face of rapid climate change, mate quality may be highly environment-dependent, and individuals might choose based on unreliable cues unless multiple cues or alternative signals are involved in choice (Heuschele et al. 2009; Head et al. 2017). For instance, increased water turbidity due to eutrophication reduced reliance on visual cues for mate quality in several fish species, leading to a greater investment in courtship and reliance on other (e.g. olfactory) cues (Candolin et al. 2007; Sundin et al. 2010; Michelangeli et al. 2015). Also, elevated water temperature was shown to change male paternal care behaviour (increased nest fanning) and resulting reproductive success via lower survival of those fathers (Hopkins et al. 2011). Plasticity, and especially TGP, could buffer some of the negative consequences of fast changing environments on mate quality cues and resulting reproductive success, since individuals pre-acclimated to specific environments should have an advantage over naive individuals (Bonduriansky & Day 2013; Head et al. 2016). Consequently, mating preference for individuals with phenotypic traits (e.g. body size, condition) optimised for specific environments via TGP could occur, leading to mate choice based on phenotype matching (assortative mating based on similar phenotype; Lacy & Sherman 1983; Jiang et al. 2013). Examples of phenotype matching are widespread, and include mate choice based on similar body size (Shine et al. 2001; McKinnon & Rundle 2002; McKinnon et al. 2004; Baldauf et al. 2009; Conte & Schluter 2013), shape (Bay et al. 2017), symmetry (Mazzi et al. 2003), colour (Milinski & Bakker 1990; Jiggins et al. 2001), behaviour, (Kitano et al. 2007), and complementary MHC genotype (important for parasite resistance; Milinski 2006; Roth et al. 2014). Nevertheless, the potential for phenotype matching based on TGP-optimised phenotypes under climate change has not yet been investigated.

Threespine stickleback, Gasterosteus aculeatus (Linnaeus, 1758), hereafter referred to simply as stickleback, is an ideal model organism to study phenotypic plasticity in general due to its high phenotypic diversity across environmental conditions (e.g. temperature, salinity, season length, habitats, predators; Bell & Foster 1994; Hendry et al. 2013), and plasticity of mate choice specifically, as its complex mating behaviour has been extensively studied for decades (Tinbergen 1951; Wootton 1984; Bell & Foster 1994; Ostlund-Nilsson et al. 2007). At the start of the breeding season, males migrate to shallow water to establish a territory and build a nest to court females to lay their eggs. The majority of eggs are fertilised by the nest owner, but alternative reproductive tactics such as sneaking and egg thievery are common (Largiader et al. 2000). Females choose among nesting males based on visual and olfactory cues signalling male quality (Candolin et al. 2016). Males display an intense red breeding coloration that has been shown to indicate overall condition, parental ability (males care for eggs and young offspring) and parasite infection status (Milinski & Bakker 1990; Eizaguirre et al. 2009). Olfactory-based mate choice experiments have further demonstrated that females prefer to mate with males with a MHC genotype that provides the optimum number of MHC variants (intermediate MHC diversity) in the offspring (Kalbe et al. 2009). Nest architecture is an extended phenotype that can also signal male quality, as nests are costly for males to maintain, and females choose nests based on their structure, location and ornamentation (Head et al. 2017). Probably the most important visual cue, however, is body size. Several studies found that females chose big males due their presumably better condition, and competitive or courting ability (Kraak et al. 1999; McLennan 2007; Jones et al. 2008; Sparkes et al. 2013). Yet, studies of stickleback species-pairs or ecotypes (e.g. benthic-limnetic, stream-lake, or anadromous-freshwater) found that females preferred males of similar size, and few interspecific or between-ecotype mating occurred between fish with conspicuous size differences (Nagel & Schluter 1998; McKinnon & Rundle 2002; Boughman et al. 2005; Kitano et al. 2007). Indeed, size-matching was found to be a more important choice factor than size itself when body size was experimentally manipulated to remove confounding effects (McKinnon et al. 2004; Conte & Schluter 2013).

Previous studies of the wild stickleback population investigated here found that body size was highly plastic in response to environmental temperature both within and across generations. Exposure to a simulated +4°C climate change scenario during development had negative effects on growth and resulting body size (Ramler et al. 2014; Schade et al. 2014; Shama et al. 2014; Shama & Wegner 2014; Shama 2015; Shama 2017). But, when mothers were acclimated to elevated temperature during reproductive conditioning, TGP resulted in (relatively) larger offspring in the +4°C climate scenario (Shama et al. 2014; Shama 2015). The mechanism underlying better growth at elevated temperature was more efficient metabolism via the inheritance of optimised mitochondria from mothers (Shama et al. 2014). Optimised mitochondrial function was underlain by changes to mitochondrial and other genes expression depending on the maternal and also grand-maternal thermal environment, suggesting an epigenetic basis for TGP (Shama et al. 2016; Ryu et al. 2018). Nevertheless, fish with a history of elevated temperature across three generations were smaller than those with an ambient temperature history (Shama & Wegner 2014), indicating that a continued increase in climate warming will likely result in smaller and smaller adult fish (see also Daufresne et al. 2009). However, bigger is not always better when environmental conditions change (Kaplan 1992). Smaller fish may be favoured under size-selective predation, or when larger size is associated with higher physiological demands under heat stress (Morrongiello et al. 2012), hence, smaller size might be more attractive under these conditions (Wong et al. 2009). Still, when body size is removed as a choice factor by size-matching potential mates, other phenotypic signals indicating mate quality in changed environments due to within-generation plasticity or TGP benefits may become important (Qvarström & Price 2001; Head et al. 2016). In this case, individuals displaying phenotypes optimised for a specific environment, for example, those with an optimised metabolism leaving more energy for reproduction, may be chosen.

Here, we investigated the role of TGP in mate choice and reproductive success of stickleback under simulated climate change in semi-natural conditions using large, outdoor mesocosms. We predicted that females should choose males with phenotypic signals indicating high quality in their specific environment, and removed body size per se as a choice factor by size-matching males and females from different TGP thermal histories (ambient and elevated temperature). Specifically, we predicted that phenotype matching based on mate quality cues and sexual traits such as body size and condition underlain by TGP benefits should lead to more mating and higher reproductive success between males and females with an ambient temperature thermal history in ambient temperature conditions, and more mating and higher reproductive success between males and females with an elevated temperature thermal history in elevated temperature conditions. By estimating reproductive success of parents with different temperature acclimation histories under changing climate conditions, we can begin to understand the role of and adaptive significance of TGP under climate change for fitness in wild populations.

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