1. A primary objective of marine ecology is to enhance our understanding of the drivers of marine fish population dynamics. These dynamics are readily understood using the framework of metapopulation ecology: for a population to persist, it must be able to self-replicate or be connected to other populations. The drivers of these criteria include rates of reproduction and dispersal, which together determine the rates of recruitment. Recruitment is, however, highly variable, and we do not know widespread patterns and causes of this variation in marine fishes. 2. Reproductive success is notoriously difficult to measure in the wild, and even more so for coral reef fishes that reside underwater. As a proxy, mating success can be predicted from more easily measured determinants, such as variation in individual traits and habitat characteristics. 3. Dispersal has, until recently, been the ‘black box’ of marine ecology, but it can be helpfully described using dispersal kernels. Currently, only five marine fishes have had their dispersal kernel empirically estimated using parentage analyses. From these studies, we see that there are at least four orders of magnitude variation in individual dispersal distances within a species. 4. Many coral reef fishes live in close association with macroinvertebrate hosts, which provide nesting sites and protection from predators. The fish themselves exhibit parental care over clutches of eggs, which hatch into dispersive larvae and recruit back into a suitable host. This life-history suggests habitat quality variation at the scale of the individual host may play a large role in determining relative reproductive and dispersal rates. To explore the role of variation in habitat quality on marine fish reproductive ecology and dispersal ecology, I perform the following three studies: 5. First, I investigate the determinants of variation in mating success in the sponge-dwelling goby, Elacatinus lori. While this fish was the first to have its larval dispersal kernel empirically measured, there were outstanding questions about its reproductive ecology. I describe the characteristics of its breeding habitat, its genetic mating system, and the correlates of male mating success. I show that sponges occupied by breeding males tend to be larger than other sponges, males exhibit a polygynous mating system, and male size, but not sponge size, is positively related to multiple metrics of male mating success. 6. Second, I test for the possibility of plasticity in larval dispersal phenotypes in response to parental habitat quality variation in the orange anemonefish, Amphiprion percula. To pursue this hypothesis, we must first establish that the conditions for parental effects to evolve are met in this system. An initial condition is whether parents can predict the habitat quality that their offspring will encounter. I test for spatial predictability of habitat quality by describing the strength and scale of spatial autocorrelation of three habitat quality indicators: anemone size, female size, and clutch size. I show that all three habitat quality indicators are positively correlated at the scale of an individual patch reef, suggesting that selection might favor parents that increase allocation to offspring that stay within the natal reef if they are in good habitat and increase allocation to offspring that travel farther and leave if they are in poor habitat. Results from this study motivate further investigation of dispersal plasticity in A. percula. 7. Third, I experimentally test the hypothesis that parents can adjust the dispersal-related traits of their offspring in response to changes in habitat quality using a lab population of Amphiprion percula. I describe changes in body size and swimming ability of offspring in response to parental habitat quality by manipulating the parents’ food rations. I find plasticity of larval body size, with parents producing larger offspring when on a low food ration than when on a high food ration. Results from this study motivate future studies to investigate plasticity of larval dispersal distances in the field. 8. In sum, I investigate how variation in habitat quality influences reproductive success, how variation in habitat quality is spatially predictable, and how variation in habitat quality influences dispersal-related traits in two important model systems in marine metapopulation ecology. The work advances our understanding of the role of habitat in determining these vital rates and population dynamics with implications for conservation and fisheries management.

Le potentiel évolutif des populations naturelles à répondre aux changements environnementaux détermine leur capacité à s'adapter et à survivre. Pour achever une évolution adaptative, la fitness doit être héritable, i.e. doit être transmise des parents à leurs descendants par des gènes. Pour pouvoir mesurer le potentiel évolutif d'une population en milieu naturel, il est primordial d'avoir au préalable des informations sur la fitness des individus qui la composent, mais aussi de connaître la fitness de leurs descendants. Les mesures de fitness sont extrêmement rares, en particulier pour les espèces marines, où les relations entre les générations sont rarement connues. Dans cette thèse, je présente le premier pedigree construit pour une population de poissons marins sur la base du suivi génétique mené depuis plus de 10 ans sur les poissons-clowns orange de l'île de Kimbe (Papouasie-Nouvelle Guinée). Le pédigrée comprend 2927 individus et révèle une philopatrie natale sur 5 générations. L'approche en génétique quantitative révèle que la fitness locale a une très faible valeur d'héritabilité (<1%). La variation génétique additive et les effets maternels sont également très faibles (<1%). En revanche, l'habitat est le principal facteur qui explique les différences de fitness locale observées entre les individus (jusqu'à 96,5%). Ensemble, ces résultats suggèrent que, bien que l'environnement impose une forte pression de sélection sur la fitness locale, la population de poissons-clowns orange a un très faible potentiel d'évolution face aux changements environnementaux. / The evolutionary potential of wild populations to respond to environmental change will determine their capacity to adapt and survive. However, in order to achieve evolutionary change, variation in the contribution of an individual to the next generation — its fitness — must have a genetic basis and be heritable. The study of the evolutionary potential of populations requires longitudinal and relatedness data with different environments to partition the contribution of genes, maternal effects and environment on fitness. Estimates of genetic heritability of fitness traits are extremely rare, especially for marine species, where inter-generational relationships are rarely known. Here, we present the first multi-generational pedigree for a marine fish population by repeatedly genotyping all individuals in a population of the orange clownfish (Amphiprion percula) at Kimbe Island (Papua New Guinea) over a 10-year period. Based on 2927 individuals, our pedigree analysis revealed that longitudinal philopatry was recurrent over five generations. We show that local reproductive success has a very low (<1%) but significant heritability. We also show that additive genetic variation and maternal effects on local fitness are both extremely low (<1%). Habitat is the major driver that explain differences in the contribution of individuals to the next generation in the local population (until 96.5%). Together these results suggest that while the environment imposes strong selection pressures on the local fitness, the low heritability indicates the orange clownfish population has little evolutionary potential to adapt to local environmental changes.

Phenotypic plasticity, the capacity of individuals to respond to changing environments by modifying traits, is critically important in allowing biological innovation in the face of environmental change. My dissertation used the clown anemonefish (Amphiprion percula) study system to explore plasticity in parenting strategies in response to variable ecological and social environments. In Part I, I investigated plasticity in response to ecological environment. First, I explored how resource variation influences parenting strategies. I measured parental behaviors in A. percula under two feeding regimes in the laboratory. I demonstrated that clownfish exhibit plasticity in parental care, and that there is significant among individual variation, i.e., personality, in parenting strategies. Second, I tested how plasticity affects life history strategies in the field. I measured habitat, reproductive, and parental traits in a natural population and found positive correlations between resource availability (anemone size) and body size, reproduction, and parental care. I conducted an experimental manipulation of resource availability and found that reproduction and parental care are plastic, providing a causal link between habitat quality variation and reproductive success in natural populations. In Part II, I investigated plasticity in response to social environment. In my third chapter, I explored how parents utilize social information to optimize their parental investment. I developed a game theory model that provides predictions for how power and punishment influence negotiations between parents over offspring care. The model predicts that the threat of punishment by a powerful parent will result in greater partner effort and, as a result, the offspring receive more total care when there is power and punishment in negotiations. Finally, I tested alternative models along with the model I developed, investigating how parents respond to each other to reach a negotiated settlement over offspring care. I experimentally handicapped one pair member and measured the response of the other parent. I found that anemonefish males and females do not respond directly to changes in their partner’s behavior, contrary to predictions of current negotiation models. Together, results from my dissertation extend our understanding of plasticity of parental care, providing a framework for understanding how parents will respond to changing environments.

Lunar cycles of reproduction are a widespread phenomenon in marine invertebrates and vertebrates. It is common practice to infer the adaptive value of this behavior based on the population level pattern. This practice may be flawed if individuals within the population are employing different reproductive strategies. Here, we capitalize on a long-term field study and a carefully controlled laboratory experiment of individually identifiable clown anemonefish, Amphiprion percula, to investigate the individual reproductive strategies underlying population-level patterns of reproduction. The field data reveal that A. percula exhibit a lunar cycle of reproduction at the population level. Further, the field data reveal that there is naturally occurring variation among individuals and within individuals in the number of times they reproduce per month. The laboratory experiment reveals that the number of times individuals reproduce per month is dependent on their food availability. Individuals are employing a conditional strategy, breeding once, twice or thrice per month, depending on resource availability. Breaking down the population level pattern by reproductive tactic, we show that each reproductive tactic has its own non-random lunar cycle of reproduction. Considering the adaptive value of these cycles, we suggest that all individuals, regardless of tactic, may avoid reproducing around the new moon. Further, individuals may avoid breeding in synchrony with each other, because of negative frequency dependent selection at the time of settlement. Most importantly, we conclude that determining what individuals are doing is a critical step toward understanding the adaptive value of lunar cycles of reproduction.

In some animal societies, access to breeding depends on the individual’s position in a hierarchy, which often depends on an individual’s size. In such societies, individuals may engage in competitive growth, trying to outgrow one another to attain a higher rank. This suggests that members of the hierarchy can track changes in the growth and size of potential competitors and respond accordingly. The clown anemonefish, Amphiprion percula, is one species known to exhibit competitive growth at the initiation of size hierarchies. Here, we use 5 combinations of sensory cues to determine which cues must be available to initiate competitive growth between size-matched individuals. Our results show that mechanosensory (pressure and/or touch) cues are used to assess size and initiate competitive growth. This study provides an understanding into the relationship between environment and phenotypic response in a social context.