Suzanne H. Alonzo

Social and coevolutionary feedbacks between mating and parental investment

A survey of empirical studies relating mating and parental investment reveals as many unpredicted patterns as results supporting existing hypotheses. This leaves us with individual post hoc explanations of observed patterns rather than an ability to make strong a priori predictions. I argue here that our ability to explain and predict empirical patterns can be improved by considering how social interactions and coevolutionary dynamics affect male and female reproductive traits. Recent research suggests that these social and coevolutionary feedbacks can increase our understanding of empirical patterns, while suggesting new directions of research. I also describe a social and coevolutionary dynamics modelling approach that integrates ideas from reproductive cooperation and sexual conflict to increase understanding of mating and parental investment.

Allocation to Mate Guarding or Increased Sperm Production in a Mediterranean Wrasse

An excellent body of literature exists that examines sperm expenditure when males allocate only to sperm production. However, in many species, males can also allocate energy to behaviors that influence sperm competition. We model whether males in sperm competition should allocate energy to mate guarding or additional sperm production. Mate guarding is predicted to lead to greater reproductive success than increased sperm output, and mate‐guarding males are not predicted to alter their allocation to sperm production with increasing sperm competition. Only when mate guarding is ineffective or greatly reduces sperm production are males predicted to allocate to sperm production. In a Mediterranean wrasse Symphodus ocellatus, three male alternative reproductive behaviors coexist. While nesting males and satellites guard mates to decrease sperm competition, sneaker males only compete via sperm production. Sneakers produce four times as much sperm per spawn as either nesting males or satellites. As predicted by the model, mate guarding but not sperm production increased with increased risk of sperm competition in nesting males. We argue that this can be explained by nesting males allocating to mate guarding rather than sperm production. Considering allocation among behaviors that affect sperm competition enhances our ability to explain and to predict sperm allocation patterns.

Mate choice games, context-dependent good genes, and genetic cycles in the side-blotched lizard, Uta stansburiana

Abstract According to mate choice models, a female should prefer males with traits that are reliable indicators of genetic quality which the sire can pass on to their progeny. However, good genes may depend on the social environment, and female choice for good genes should be context dependent. The side-blotched lizard, Uta stansburiana, exhibits genetically based throat colors (orange, blue, or yellow) that could be used as a sexually selected signal since they reliably predict the genetic quality of mates. The frequencies of male and female morphs cycle between years, and both male and female morphs have an advantage when rare; thus genetic quality will depend on morph frequency. A female should choose a sire that maximizes the reproductive success of both male and female progeny. We examine a game theoretical model that predicts female mate choice as a function of morph frequency and population density. The model predicts the following flexible mate choice rule: both female morphs should prefer rare males in ’boom years’ of the female cycle (e.g., ’rarest-of-N rule’), but prefer orange males in ’crash years’ of the female cycle (’orange-male rule’). Cues from the current social environment should be used by females to choose a mate that maximizes the future reproductive success of progeny, given the social environment of the next generation. We predict that the cue is the density of aggressive orange females. In the side-blotched lizard, cycling mate choice games and context-dependent mate choice are predicted to maintain genetic variation in the presence of choice for good genes.

Female mate choice copying affects sexual selection in wild populations of the ocellated wrasse

Explaining the factors that determine the distribution of mating success among males is essential to our understanding of sexual selection. Classic theory has focused on how competition among males and female choice for traits of the male or his territory drive sexual selection. Recent theory has also shown that female mate choice copying can alter the strength and direction of selection on male traits. Yet, we know very little about the prevalence and importance of nonindependent female choice in wild populations. In a species with male territoriality and paternal care (the ocellated wrasse, Symphodus ocellatus), I first show that females express nonindependent mate choice, responding both to the recent mating success of the male and to the presence of other spawning females rather than to variation in male courtship or defence of the nest. Females were significantly more likely to spawn with the same male when another spawning female was present than when they were alone at the nest, providing some of the first direct evidence of female mate choice copying under natural conditions in the wild. I further show that a short-term experimental increase in a territorial males mating success attracts more females in the future and increases male paternal care. These observed patterns of female choice and male care are consistent with female choice for the direct benefits of male care where the best indicator trait of male parental effort is the mating behaviour of other females rather than male courtship behaviour or physical traits.

Sexual selection and alternative mating behaviours generate demographic stochasticity in small populations

Recent theory predicts that environmental variation and small population size facilitate the coexistence of alternative phenotypes despite unequal mean fitness. However, traditional studies of reproductive strategies often assume that the stability of alternative mating behaviours relies on equal male fitness. We present results from field observations and experimental manipulations of thermal resources on territories demonstrating the coexistence of alternative reproductive behaviours with unequal fitness. The side–blotched lizard Uta stansburiana exhibits two alternative strategies for territoriality:‘usurp’ and‘defend’. Paternity analysis revealed significantly greater mean fitness for‘usurpers’ than‘defenders’ in our study of natural variation. Moreover, variance in fitness was significantly higher for usurpers on both experimental and natural plots, implying that‘usurp’ is a risky strategy with potentially large pay–offs or none at all. We show theoretically that significantly higher variance in usurper fitness can allow for coexistence with defenders despite higher mean fitness of usurpers. This coexistence is facilitated by small population size. Our results have general implications for the evolution of alternative strategies and the maintenance of genetic diversity in small populations.

ECOLOGICAL GAMES IN SPACE AND TIME: THE DISTRIBUTION AND ABUNDANCE OF ANTARCTIC KRILL AND PENGUINS

The distribution and abundance of organisms are affected by behaviors, such as habitat selection, foraging, and reproduction. These behaviors are driven by interactions within and between species, environmental conditions, and the biology of the species in- volved. Although extensive theoretical work has explored predator-prey dynamics, these models have not considered the impact of behavioral plasticity and life-history trade-offs on predicted patterns. We apply a modeling method that allows the consideration of a spatial, dynamic ecological game between predators and prey using a life-history perspec- tive. As an illustrative example, we model the habitat selection of Antarctic krill and penguins during the time when penguins are land-based for reproduction. Although envi- ronmental conditions and the life-history constraints of each species have both direct and indirect effects on both species, the penguins foraging rule (whether food-maximizing or time-minimizing) has the greatest effect on the qualitative distribution pattern of both species. Size-dependent diel vertical migration of krill also strongly affects penguin foraging patterns. This model generates suggestions for future research and qualitative predictions that can be tested in the field. The application of this method to a specific problem also demonstrates its ability to increase our understanding of important ecological interactions

Sexual selection favours male parental care, when females can choose

Explaining the evolution of male care has proved difficult. Recent theory predicts that female promiscuity and sexual selection on males inherently disfavour male care. In sharp contrast to these expectations, male-only care is often found in species with high extra-pair paternity and striking variation in mating success, where current theory predicts female-only care. Using a model that examines the coevolution of male care, female care and female choice; I show that inter-sexual selection can drive the evolution of male care when females are able to bias mating or paternity towards parental males. Surprisingly, female choice for parental males allows male care to evolve despite low relatedness between the male and the offspring in his care. These results imply that predicting how sexual selection affects parental care evolution will require further understanding of why females, in many species, either do not prefer or cannot favour males that provide care.

Male Fecundity Stimulation: Conflict and Cooperation Within and Between the Sexes: Model Analyses and Coevolutionary Dynamics

Female promiscuity forces the ejaculates of different males to compete for fertilization through sperm competition. In turn, competing ejaculates often influence female promiscuity and fitness, for example, when ejaculate products increase female fecundity. Here we develop theory examining situations where males stimulate female fecundity and compete for fertilization and female remating is influenced by male fecundity stimulation. We consider the fitness consequences that fecundity stimulation has simultaneously for males inseminating the same female and for the female herself, and we show that the way fecundity increases with male stimulation shifts the coevolutionary dynamics of female remating and male ejaculate expenditure from conflict to cooperation among all mating partners. When fecundity stimulation is weak and males “know” their mating roles, the second male to inseminate a female can exploit the fecundity stimulation of the first male, fostering intra‐ and intersexual conflict over female remating. However, in a diversity of species where fecundity more than doubles with remating, we show that the female and both males can gain from female remating, leading to intra‐ and intersexual cooperation over female remating. This coevolutionary perspective yields new insights into the connection between promiscuity, fecundity, and sperm competition and the complex interplay between sexual conflict and cooperation.

Why Do Cuckolded Males Provide Paternal Care

A comparative analysis across insects, birds, fish, and mammals reveals why it sometimes pays for males to care for the offspring of other males.

The unexpected but understandable dynamics of mating, paternity and paternal care in the ocellated wrasse

Although theory generally predicts that males should reduce paternal care in response to cues that predict increased sperm competition and decreased paternity, empirical patterns are equivocal. Some studies have found the predicted decrease in male care with increased sperm competition, while even more studies report no effect of paternity or sperm competition on male care. Here, we report the first example, to our knowledge, of paternal care increasing with the risk and intensity of sperm competition, in the ocellated wrasse (Symphodus ocellatus). Theory also predicts that if paternal care varies and is important to female fitness, female choice among males and male indicators traits of expected paternal care should evolve. Despite a non-random distribution of mating success among nests, we found no evidence for female choice among parental males. Finally, we document the highest published levels of extra-pair paternity for a species with exclusive and obligate male care: genetic paternity analyses revealed cuckoldry at 100 per cent of nests and 28 per cent of all offspring were not sired by the male caring for them. While not predicted by any existing theory, these unexpected reproductive patterns become understandable if we consider how male and female mating and parental care interact simultaneously in this and probably many other species.