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Seasonal Interactions Between Photoperiod and Maternal Effects Determine Offspring Phenotype in Franklin’S Gull

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Seasonal Interactions Between Photoperiod and Maternal Effects Determine Offspring Phenotype in Franklin’S Gull Functional Ecology 2012, 26, 948–958 doi: 10.1111/j.1365-2435.2012.02010.x Seasonal interactions between photoperiod and maternal effects determine offspring phenotype in Franklin’s gull Mark E. Clark* and Wendy L. Reed Department of Biological Sciences, North Dakota State University, P.O. Box 6050, Dept. 2715, Fargo, North Dakota, 58108-6050 USA Summary 1. When predictable seasonal changes affect offspring fitness, we expect offspring to evolve phe- notypes that minimize the costs of seasonal variation in timing of breeding. For species with parental care during embryonic development, offspring receive seasonal cues of the environ- ment from parents that are biased by their parent’s fitness (which is not equivalent to offspring fitness). Therefore, mechanisms enabling offspring to detect environmental cues independent of parents should be strongly favoured. 2. We experimentally evaluated the ability of avian embryos to integrate cues of season from photoperiod and maternal environments present in eggs to produce seasonal variation in phe- notypes among Franklin’s gull (Leucophaeus pipixcan) hatchlings. Eggs were collected early and late in the season and some were separated into their component parts and others were incubated under short (early season) and long (late season) photoperiods. After hatching, we measured the structural size of the chicks and the amount of yolk sac reserves. 3. We found that hatchling size, a phenotype linked with fitness, is sensitive to both egg con- tents provided by mothers and photoperiod, and development time decreases across the sea- son. The effects of integrating cues of season from eggs and photoperiod on offspring phenotype are complex, and when cues of season from eggs are mismatched with cues of sea- son from photoperiod, alternate phenotypes are created. 4. We also found that seasonal variation in egg size, yolk, albumen or shell content of the eggs do not account for the seasonal maternal egg effect on hatchling size. This seasonal maternal effect could be a result of other egg constituents or reflect heritable variation in timing of breeding that is linked with offspring size. 5. Changes in breeding phenology of adults could result in a mismatch between cues from par- ents and photoperiod cues of season. For example, if breeding seasons advanced such that late season birds initiate breeding at an early season photoperiod, offspring would then be integrat- ing maternal cues of late season with photoperiod cues of early season and alter their pheno- types. We expect our results to initiate new studies on how vertebrate embryos integrate environmental cues with maternal effects and offspring responses to optimize the expression of offspring phenotype. Key-words: avian, embryonic development, Leucophaeus pipixcan, life-history trade-offs, parent–offspring conflict, phenotypic plasticity, photoperiodism, seasonality organisms (Bradshaw & Holzapfel 2007). In temperate Introduction regions, seasonal increases in temperature, water and Animals exploiting seasonal environments take advantage energy provide times for which fitness is maximized by of regular changes in resources, which are responsible for reproduction and rearing young, whereas decreases in these organizing biological processes and the annual cycle of resources result in times when fitness is maximized by migration or quiescent life-history phases. The ability to *Correspondence author. E-mail: [email protected] predict seasonal changes correctly and initiate appropriate © 2012 The Authors. Functional Ecology © 2012 British Ecological Society Seasonal effects on offspring phenotype 949 behavioural, physiological and biochemical responses that have a higher likelihood of survival than offspring pro- maximize fitness is shaped by natural selection (Bradshaw duced late in the season (Moreno 1998; Drent 2006; Ver- & Holzapfel 2007; Lyon, Chaine & Winkler 2008). Photo- hulst & Nilsson 2008). Parents are predicted to favour period provides a consistent cue of season that animals use offspring with higher likelihood of survival, especially to predict optimal timing for annual events (Bradshaw & when allocation of resources to offspring with low likeli- Holzapfel 2007; Lyon, Chaine & Winkler 2008), and the hood of survival decreases future reproductive potential of refinement of timing of breeding within a season is pro- parents [i.e. the reproductive constraint hypothesis (Win- vided by additional biotic and abiotic cues (Wingfield & kler 1987; Stearns 1992; Verhulst & Nilsson 2008)]. The Kenagy 1991; Visser, Holleman & Caro 2009; Visser et al. consequences of seasonal variation in reproduction have 2011). The influence of photoperiod in orchestrating sea- been considered mainly from the perspective of conse- sonal changes in adult phenotype has a long history of quences for parental fitness and trade-offs between current study, but the influence of photoperiod and season on juve- and future offspring. In seasonal environments, parents nile phenotype has been little explored outside invertebrate must transition from breeding to preparation for migration systems (Dmitriew 2011). and winter. Offspring and parental fitness, however, are A rich body of literature documents the influence of sea- not equivalent (Wolf & Wade 2001; Mu¨ller et al. 2007) son and photoperiod on producing adaptive phenotypes in and the consequences of season on current offspring fitness juvenile and larval invertebrates (Kingsolver & Huey 1998; are large. Offspring are under similar seasonal time con- Bradshaw & Holzapfel 2010; Sniegula & Johansson 2010; straints as adults as well as additional constraints; that is, Beldade, Mateus & Keller 2011). However, the life histo- they must grow, develop and moult, as well as learn to for- ries of many of these invertebrates (i.e. mosquitos, pea age and fly to be ready to migrate. When the costs of sea- aphids and butterflies) do not include parental care. In the sonal timing are high for offspring, we expect offspring to absence of parental care, juveniles interact directly with evolve mechanisms to detect timing of season, and mecha- their environments, which minimizes any conflict between nisms to mitigate negative fitness consequences of seasonal offspring and parent because the offspring phenotype is variation in timing of breeding. unlikely to affect future reproductive success of parents. In Examining the effect of seasonality on offspring fitness is contrast, when parents provide prenatal or natal care, particularly relevant in birds, which have served as a criti- embryos and juveniles experience environments as trans- cal model and indicator of shifts in timing of seasonal lated by or through parents and the offspring phenotype events (Lyon, Chaine & Winkler 2008). Consistent changes can directly affect future reproductive success of parents. in temperatures across local and global scales are affecting For example in mammals, photoperiods experienced by annual cycles of plants and animals (Bradshaw & Holzap- females can be translated to their foetuses through changes fel 2008); however, photoperiod is not labile. The extent to in maternal hormones, resulting in long-term effects on off- which a mismatch between photoperiodic cues of season spring life-history traits (Horton 2005) and adult condition and temperature driven changes in seasonality affects bio- (French et al. 2009). Such maternal effects are also present logical systems requires knowledge of the mechanisms by in oviparous animals, although direct exchange of mater- which organisms sense and respond to seasonal environ- nal resources with offspring is limited to a short period of ments. Avian embryos are capable of sensing and respond- time prior to oviposition (Schwabl 1996b; Groothuis & ing to photoperiod as demonstrated in poultry (Siegel Schwabl 2008). Bird eggs contain maternally derived et al. 1969b; Shafey 2004a), but has only recently been androgens (Reed & Vleck 2001; Groothuis et al. 2005; explored as an adaptive mechanism affecting incubation Boonstra, Clark & Reed 2009), melatonin (Bozenna et al. period in wild populations (Cooper et al. 2011). Current 2007), thyroid hormones (Wilson & McNabb 1997), anti- hypotheses of photoperiod effects on avian embryonic bodies (Grindstaff, Brodie & Ketterson 2003), carotenoids development focus on the function of day length in setting (Newbrey & Reed 2009), vitamins (Biard et al. 2009) and the circadian rhythm in the final stages of incubation RNA transcripts (Knepper et al. 1999; Malewska & Ols- (Nichelmann, Hochel & Tzschentke 1999; Okabayashi zanska 1999), all of which are biologically active, poten- et al. 2003), photo acceleration of development (reviewed tially affect embryonic growth and development and can in Cooper et al. 2011; and Reed & Clark 2011) and photo- vary seasonally (Watanabe et al. 2007; Hargitai et al. periodic effects on post-hatching growth in artificially 2009). Although birds have played a critical role in evalu- incubated poultry (Rozenboim et al. 2003). ating both the impacts of maternal provisioning on off- Under the reproductive constraint hypothesis, animals spring (Groothuis et al. 2005) and changes in adult that are long-lived, undergo long migrations and provide phenology in response to changing seasons (Lack 1950; parental care are expected to invest more in their own sur- Perrins 1970), the ability of avian embryos to integrate vival at a cost to their current offspring when those off- both maternal and photoperiod cues of season has not spring have a low probability of survival (Winkler 1987; been explored. Stearns 1992). Gulls
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