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The Importance of Nutrition in Sexual Selection

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The Importance of Nutrition in Sexual Selection Food for Thought: The Importance of Nutrition in Sexual Selection Submitted by James Ian Leonard Rapkin, to the University of Exeter as a thesis for the degree of Doctor of Philosophy in Biological Sciences in November 2016 This thesis is available for library use on the understanding that it is copyright material and that no quotation from the thesis may be published without proper acknowledgment. I certify that all materials in this thesis that are not my own work have been identified and that no material has previously been submitted and approved for the award of a degree by this or any other University. PHD THESIS 2016 James I. L. Rapkin i ABSTRACT Sexual selection and sexual conflict are two fundamental evolutionary mechanisms that are responsible for the diversification of a range of morphological, behavioural and physiological traits in the sexes, across most animal taxa. Decades of empirical research has shown that the expression of many (if not all) of these traits is dependent on diet. Few studies have, however, provided a detailed view of how diet influences the operation of sexual selection and sexual conflict. The traditional view that nutritional resources are of a single form, namely energy or calories, has recently been challenged by the idea that it is the combination of various micro- and/or macronutrients that is key to trait expression and in maintaining reproductive fitness. While this established dogma is changing, more empirical studies are needed that focus on the how the intake of specific nutrients influence the expression of key traits that regulate the operation of sexual selection and sexual conflict. In this thesis I examine the role of nutrition on the operation of sexual selection and sexual conflict. To achieve this I perform a number of experiments utilising the Geometric Framework (GF) of nutrition to tease apart specific effects of two macronutrients (protein and carbohydrates) on a number of important phenotypic traits in two field cricket species; the decorated cricket Gryllodes sigillatus and the Australian black field cricket Teleogryllus commodus. I also combine the GF with conventional quantitative genetic experiments to examine the potential for the genetics of dietary choice to constrain the evolution of key traits that regulate sexual selection and sexual conflict. I start by examining the effect of protein (P) and carbohydrate (C) intake on a male sexual trait, the cuticular hydrocarbon (CHC) profile, known to be subject to strong pre- copulatory sexual selection in G. sigillatus. I find that diet influences the expression of male CHCs and how attractive a male is to a female. Specifically, I show that CHCs are maximized at a high intake of nutrients in a P:C ratio of 1:1.5, that female pre-copulatory choice exerts significant selection on this variation in male CHCs and that the nutritional optima for male mating success almost perfectly matched the optima for CHC expression. However, this change in CHC expression was not the only pathway for the effects of nutrient intake on male pre-copulatory attractiveness to females suggesting that other trait(s) are also important in mediating this relationship (Chapter 2). Next, I examine the effect of the intake ii of these nutrients on the regulation of sexual conflict in G. sigillatus. Males in this species produce a large, gelatinous nuptial gift (the spermatophylax) that the female consumes during mating and that prevents her from prematurely removing the sperm-containing ampulla and terminating mating. The size and amino acid composition of the spermatophylax are known to prolong the attachment time of the ampulla and, therefore, prevent the female from exerting post-copulatory mate choice. I show that the size and amino acid composition that increases the gustatory appeal of the spermatophylax to females is maximised at a high intake of nutrients in a P:C ratio of 1:1.3 (Chapter 3). Furthermore, I show that the nutritional optima for these properties of the spermatophylax are almost perfectly aligned with the optima for ampulla attachment time. This suggests that the balanced intake of P and C is fundamental to the regulation of sexual conflict in this species. A key assumption in life-history theory is that phenotypic traits important to fitness will be subject to trade-offs as they compete for a limited pool of resources. In most empirical studies, the nutrients in food are considered the resource that life-history traits compete for during development, yet the diets provided are typically poorly resolved so that the specific nutrients regulating any trade-off cannot be determined. While the GF provides a powerful way to examine how specific nutrients influence the trade-off between traits, this framework currently lacks a robust protocol to quantify the presence and magnitude of nutritionally based trade-offs. In Chapter 4, I start by developing a standardized protocol for quantifying the presence and magnitude of nutritionally based trade-offs when using the GF. This work shows that nutritionally based trade-offs occur when life-history traits are maximised in different regions of nutrient space and that this divergence can be quantified by the overlap in the 95% confidence region (CR) of the global maxima, the angle (θ) between the linear nutritional vectors and the Euclidean distance (d) between the global maxima for each trait. As these metrics are measured in a standardized way, they can be directly compared across different traits, the sexes and model organisms. Next, I test this protocol by examining the nutritional basis of the trade-off between reproductive effort and immune function in male and female G. sigillatus. I show that encapsulation ability and egg production in females increased with the intake of both nutrients, being maximised at a P:C ratio of 1.04:1 and 1:1.17, respectively. In contrast, encapsulation ability in males only increased with the intake of P being maximised at a P:C iii ratio of 5.14:1, whereas calling effort increased with the intake of C but decreased with the intake of P and was maximized at a P:C ratio of 1:7.08. Consequently, the trade-off between reproduction and encapsulation ability is much larger in males than females and this is supported by the non-overlapping 95% CRs on the global maxima for these traits in males and the larger estimates of θ and d. Sexual selection promotes the evolution of sex differences in life history strategies and this often requires different intakes of nutrients. Indeed, the sexes in many different species have evolved divergent nutritional optima for a range of important fitness-related traits. If dietary choice for the intake of these nutrients is genetically uncoupled in the sexes, males and females should evolve sex differences in nutrient intake and each sex should evolve to their sex-specific nutritional optima. However, if the sexes have different nutritional optima but dietary choice is positively genetically correlated between the sexes, this will constrain the evolution of sexual dimorphism in nutrient intake and prevent one or both sexes from reaching their nutritional optima: a process known as intralocus sexual conflict (ISC). In Chapter 5, I examine the potential for ISC over the optimal intake of nutrients for reproduction and lifespan in male and female black field crickets, T. commodus. I show that males and females have distinct dietary optima for lifespan and reproductive effort. Male lifespan and nightly calling effort were both maximised at a high intake of nutrients in a P:C ratio of 1:8, whereas female lifespan and daily egg production were maximised at a high intake of nutrients in a P:C ratio of 1:2 and 1:1, respectively. Using a half-sib quantitative genetic breeding design I also showed positive genetic correlations between the intake of P and C in the sexes. Together this provides the potential for ISC over the optimal intake of nutrients to influence the evolution of sexual dimorphism in reproductive effort and lifespan. However, by measuring the genetic constraint (which compares the predicted evolutionary response of these traits when there is genetic covariance between the sexes for nutrient intake, to the predicted response when the genetic covariance is set to zero (i.e. no genetic constraint)), I show that the positive genetic correlations over nutrient intake had little effect on the predicted response of nutrient regulation in the sexes. Furthermore the within sex, additive genetic variance-covariance matrix appeared to play more of a role in constraining the predicted response of nutrient regulation in the sexes. iv When presented with a nutritionally imbalanced diet, animals often show a range of compensatory feeding behaviours to increase their intake of any nutrient(s) that are deficient. However, such behaviours may come at a cost, as the more common nutrients are over-consumed and may impact homeostatic functioning and health. Due to the different nutritional demands of reproduction in the sexes, males and females often show different compensatory feeding behaviours that target different nutrients and this has been shown to have differential health consequences in the sexes. Little is known, however, about the role that genes play in this process: are the sexes genetically predisposed to under or over-ingest nutrients when encountering a nutritionally imbalanced diet and is any genetic predisposition for dietary regulation linked to genes for health in the sexes? In my final chapter (Chapter 6), I examine the quantitative genetics of dietary choice in male and female T. commodus and the potential health consequences this may have in terms of lipid deposition. Using a split-brood breeding design, where different full-sibling offspring of each sex were provided with alternate pairs of imbalanced diets, I showed significant genotype- by-sex and genotype-by-diet pair interactions for the total diet consumed, the total preference for nutrients and lipid deposition.
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