Barry Sinervo

Traditional life history theory ignores trade-offs due to social interactions, yet social systems expand the set of possible trade-offs affecting a species evolution by introducing asymmetric interactions between sexes, age classes, and invasion of alternative strategies. This chapter outlines principles for understanding mechanisms underlying gene epistasis due to signaller–receiver dynamics, gene interactions between individuals, and impacts on life history trade-offs.

Traditional life history theory ignores trade-offs due to social interactions, yet social systems expand the set of possible trade-offs affecting a species evolution--by introducing asymmetric interactions between the sexes, age classes and invasion of alternative strategies. We outline principles for understanding gene epistasis due to signaller-receiver dynamics, gene interactions between individuals, and impacts on life history trade-offs. Signaller-receiver epistases create trade-offs among multiple correlated traits that affect fitness, and generate multiple fitness optima conditional on frequency of alternative strategies. In such cases, fitness epistasis generated by selection can maintain linkage disequilibrium, even among physically unlinked loci. In reviewing genetic methods for studying life history trade-offs, we conclude that current artificial selection or gene manipulation experiments focus on pleiotropy. Multi-trait selection experiments, multi-gene engineering methods or multiple endocrine manipulations can test for epistasis and circumvent these limitations. In nature, gene mapping in field pedigrees is required to study social gene epistases and associated trade-offs. Moreover, analyses of correlational selection and frequency-dependent selection are necessary to study epistatic social system trade-offs, which can be achieved with group-structured versions of Price's (1970) equation.

Reproduction is thought to entail costs, but assessing survival costs associated with maturation as organisms express reproductive genes for the first time is problematic because many will die prior to expressing a phenotype. We quantified selection acting on this invisible fraction by measuring selection on predicted breeding values for clutch size estimated from a multigenerational pedigree of side-blotched lizards in which clutch size was heritable (h2=0.25+/-0.04). The survival effects of predicted breeding values for clutch size during maturation, however, differed between males and females indicating ontogenetic conflict. Increased mortality during maturation was associated with lower predicted breeding values for clutch size for females, but higher predicted breeding values for males who do not produce a clutch. Genetic correlations between clutch size and male and female survival were consistent with calculated selection differentials. Experimental yolk removal did not affect progeny survival during maturation, indicating that selection on maturing progeny was not due to confounding yolk-volume maternal effects, and hormone manipulations confirmed clutch size as the target of viability selection during maturation. Such episodes of selection prior to phenotypic expression of the trait will have important consequences for the evolution of reproductive investment.

Maternal effects facilitate adaptation to changing environments because they alter individual offspring traits to match current conditions. We show that maternal effects can also resolve context-dependent, correlational selection on multiple offspring traits, promoting adaptation to more complex environments. In side-blotched lizards (Uta stansburiana), two alternative pathways of dorsal pattern induction involve maternal oestradiol and alleles for throat colouration (� social strategy). In one pathway, females increased yolk oestradiol when mated to yellow-throated sires; oestradiol induced dorsal barring in yellow-throated progeny of both sexes. In another pathway, females elevated yolk oestradiol in response to a high frequency of orange alleles in experimental social neighbourhoods. When the sire lacked yellow alleles, this secondary pathway resulted in striped, orange sons and striped, non-orange daughters. All maternally induced types had high fitness in the wild. These results illustrate a (previously undescribed) mechanism for females to simultaneously resolve differing correlational selection pressures on different progeny.

Abundant evidence suggests that females may engage in mate choice to gain nongenetic (material) benefits from high-quality territories; however, the selective consequences that influence those choices are not well understood. We studied the fitness effects of territory quality and incubation temperature on juvenile lizards in nature. We manipulated territory quality by redistributing rocks between pairs of neighboring home ranges. Rock manipulations set up adjacent plots that were either experimentally improved or reduced in quality. We incubated eggs from field-caught gravid females in each of three temperature treatments in the laboratory (low, medium, and high temperature). Progeny were released in either experimentally improved or reduced-quality plots upon hatching, and the following spring we measured survival as a function of egg size and laying date. We conducted concurrent studies of the thermal environment on experimental territories. Improved territories provided significantly more hours for lizards to behaviorally thermoregulate at their preferred body temperature and also provided nest sites with incubation conditions that were closer to optimal compared with reduced-quality plots. Reduced-quality plots were significantly more variable in quality. Finally, we measured significant correlational selection between egg mass and laying date on manipulated plots in two separate years. Results indicate the influence of environmental variation on correlational selection on life-history traits.

We describe new ESS models of density regulation driven by genic selection to explain the cyclical dynamics of a social system that exhibits a rock‐paper‐scissors (RPS) set of three alter...

Altruism presents a challenge to evolutionary theory because selection should favor selfish over caring strategies. Greenbeard altruism resolves this paradox by allowing cooperators to identify individuals carrying similar alleles producing a form of genic selection. In side-blotched lizards, genetically similar but unrelated blue male morphs settle on adjacent territories and cooperate. Here we show that payoffs of cooperation depend on asymmetric costs of orange neighbors. One blue male experiences low fitness and buffers his unrelated partner from aggressive orange males despite the potential benefits of defection. We show that recognition behavior is highly heritable in nature, and we map genetic factors underlying color and self-recognition behavior of genetic similarity in both sexes. Recognition and cooperation arise from genome-wide factors based on our mapping study of the location of genes responsible for self-recognition behavior, recognition of blue color, and the color locus. Our results provide an example of greenbeard interactions in a vertebrate that are typified by cycles of greenbeard mutualism interspersed with phases of transient true altruism. Such cycles provide a mechanism encouraging the origin and stability of true altruism.

We assessed genetic factors on progeny dispersal due to sire color morph genotypes in a field pedigree and lab crosses, and we measured maternal effects by studying both natural and experimentally induced egg size variation. Progeny were released into nature upon hatching, but we recorded dispersal distance at maturity, which reflects effective dispersal after viability selection has run its course. Progeny dispersal was significantly affected by sire genotype. Progeny from orange sires dispersed the farthest. Progeny from blue sires dispersed intermediate distances. Progeny from yellow sires were the most philopatric. Sire genotype effects interacted with egg size. In particular, enlarged progeny from orange sires dispersed farther, while enlarged progeny from yellow sires were more philopatric. Progeny from blue sires were unaffected by egg size manipulations. Egg manipulations and natural variation generally had concordant effects indicative of causation. However, asymmetry of gigantization and miniaturization on progeny dispersal from some sire genotypes suggest the involvement of maternal factors besides egg size. Results of laboratory crosses with progeny released into nature confirmed key sire genotype effects and identified additional maternal effects that modulated dispersal as a function of progeny gender. We discuss the adaptive implications of progeny dispersal in the context of male (rock‐paper‐scissors) and female strategies (r‐ and K‐density cycle) that are associated with color morphs.

Ontogenetic conflict arises when optima for alleles governing fitness variation differ between juveniles and adults or between adult sexes. Loci that govern development of alternative phenotypes in the sexes, hereafter termed morph-determining loci, mediate development through the endocrine system. Morphotypic selection is defined to be multivariate selection favoring discrete alternative morphotypes (e.g., optima). When the optimal combinations of alleles for alternative morphs differ between the sexes, it generates conflicting selection pressure and thus ontogenetic conflict. Selection on morph alleles promotes ontogenetic conflict because it perturbs physiological epistasis that governs the expression of male versus female traits. Expression of physiological traits arises from homeostasis that maintains trait expression within a normal range. The genetic basis of homeostasis is likely to arise from interactions among several genes (e.g., genetic epistasis) or protein products (e.g., physiological epistasis). For example, endocrine regulation arises from interactions between gondatropins, which are protein hormones produced by the hypothalamic-pituitary glands, and steroid hormones, which are produced by the gonads (e.g., HPG axis). The side-blotched lizard system is discussed with respect to physiological bases of ontogenetic conflict. We also describe a novel molecular marker strategy for uncovering genome-wide physiological epistasis in nature. Finally, ontogenetic conflict exerts selection on females to evolve mate selection or cryptic choice that is reflected in different sires being chosen for son versus daughter production. We describe how side-blotched lizard females ameliorate ontogenetic conflict by cryptic choice of male genotypes to produce sons versus daughters.