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.

Species that vary in social structure within and among populations can provide unparalleled insight into the evolution of sociality. The theridiid spider Anelosimus studiosus varies widely in its social structure at the northern edge of its range. Colony sizes range from the solitary/territorial female with her offspring to cooperative colonies of tens to hundreds of adult females. In previous work, we developed an assured fitness returns 'brood-fostering model' that predicts that in cooler environments mothers in multiple-female colonies will have a selective advantage over solitary female nests. According to the model, at cool sites the rate of juvenile maturation is slowed, increasing the probability that the mother will die before the brood reaches independence. In her absence, other females would foster her brood. We tested this hypothesis by manipulating colony size and by monitoring the reproductive success of naturally occurring solitary and multifemale colonies in cold and warm temperature environments. Our results indicate that while multiple-female colonies have higher fitness at cool sites, the solitary female nests achieve higher fitness at warmer sites. The higher reproductive success of multifemale colonies at cold sites further reflects the total failure of solitary female nests at these sites. Solitary female nests that survived generally had higher reproductive success than multifemale colonies at all temperatures. In natural colonies, fitness was highest for smaller multifemale colonies in the colder environments and decreased in the larger colonies. We use these data to refine the brood-fostering model and discuss the results with regard to the observed polymorphism in social structure.

京都大学 / 0048 / 新制・課程博士 / 博士(理学) / 甲第18104号 / 理博第3982号 / 新制||理||1574(附属図書館) / 30962 / 京都大学大学院理学研究科生物科学専攻 / (主査)准教授 森 哲, 教授 沼田 英治, 教授 疋田 努 / 学位規則第4条第1項該当 / Doctor of Science / Kyoto University / DGAM

Parental care can be important especially in passerine birds and can depend on environment, food availability and behaviour. A behaviour that can affect the food supply for the offspring is neophobia, the fear of novel objects. The more fear the bird exhibits the less it visits the nest with food. In my study I aimed to examine neophobia and how it differed based on sex and if offspring number and weight influenced the behaviour. Video recordings of collared flycatchers nest boxes were used to see how the behaviour differed by placing a novel object on the nest box. The behaviours tested were duration of perching, hovering and visit including latency and frequency of visit. The results showed that there was a significant difference between the sexes in duration, latency, and frequency of visit but also duration of perching before and after placing a novel object on the nest box. In addition, my results showed that nestling weight significantly influenced frequency of visit and nestling number influenced duration of visit. The study shows that the collared flycatchers do express neophobia differently based on the sex and the nestling’s weight and number. Future studies could investigate if neophobia is a plastic behaviour and the effects of prolonged exposure to novel objects whichcould change the offspring’s survival chances or even the nestling’s behaviour.

Cannibalism of offspring is a common yet seemingly paradoxical phenomenon observed across a wide variety of taxa. Behavioural ecologists have been particularly interested in understanding this behaviour within the context of parental care. This is because, superficially, offspring cannibalism appears counterproductive to the goals of a caring parent, which are often achieved by nurturing and protecting their young. Despite the prevalence of offspring cannibalism in many taxa, we still have a poor evolutionary understanding of this intriguing behaviour. Many hypotheses have been proposed explaining why parents may terminate and consume offspring, however, empirical tests of these hypotheses frequently return mixed results, and few examples exist in which multiple hypotheses for cannibalism have been tested using the same model study system. Over the course of my PhD thesis, I tested different cannibalism hypotheses in a novel study organism, the plainfin midshipman fish (Porichthys notatus), a species of paternal care-giving toadfish that frequently engages in offspring cannibalism. I first characterized the factors that underlie male reproductive success in this species to provide a broader understanding of their reproductive ecology and a background for the cannibalism studies in my later chapters. I showed that both male size and nest size are important correlates of male reproductive success (e.g. mate attraction, egg acquisition, and rearing success) in this system, and that morphological, physiological, and ecological variables can also have an impact on reproductive success (Chapter 2). Next, I conducted a series of field and laboratory studies to uncover the factors that select for offspring cannibalism in this species. In particular, I investigated whether offspring cannibalism serves to replenish dwindling energy reserves and/or occurs when paternity over a brood is likely to be low. I showed that although plainfin midshipman males endure a long and energetically taxing parental care period, they cannibalize offspring most frequently early in the breeding season, the time period when the males are in their best body condition but when male-male competition is also at its peak (Chapter 3). Using a direct comparison of males that had recently cannibalized offspring versus those that had not, I showed that the males with the lowest energy reserves were actually the least likely to have offspring in their digestive tracts, suggesting that offspring cannibalism is not driven by immediate energetic need (Chapter 4). I then tested whether males assess their paternity using direct or indirect offspring cues, and showed that males use the act of a nest take-over as reliable indirect cues of their paternity over a brood (Chapter 5). Altogether, my results further our understanding of the reproductive ecology of the plainfin midshipman fish, and provide a foundation upon which to assess and test between cannibalism hypotheses in this species and others. My thesis work demonstrates the advantage of studying multiple cannibalism hypotheses in a single study system, and through this approach we can gain a more accurate evolutionary understanding of how the phenomenon of offspring cannibalism is maintained in different species. / Thesis / Doctor of Philosophy (PhD)

Behavioral traits can be remarkably flexible depending on the conditions in which they are expressed, yet, in spite of this flexibility, persistent differences between individuals appear to limit the potential expression of behaviors. For example, despite evidence that parents provide variable amounts of parental care in response to changing environmental conditions, they also differ in the overall level of care they provide. I used a behavioral reaction norm approach to study individual variation in parental care behavior in free-living house sparrows (Passer domesticus). I investigated the nature of this variation by studying the relationship between different forms of parental care, the biological basis of individual variation in care, and the effect of this variation in care on offspring. First, I found a positive covariance between nestling provisioning and nest defense. Parents that provided high levels of care in one context provided high levels of care in the other context, even after accounting for measures of offspring value. Second, I sought to identify the biological sources that create and maintain consistent individual differences in the level of care a parent provides. I found that the likelihood of feeding nestlings large food items was positively associated with genetic heterozygosity, but did not find evidence that nestling provisioning was influenced by additive genetic variation in this population. Parents hatched from larger eggs provisioned offspring at a higher rate than parents hatched from smaller eggs, but there was no effect of other conditions experienced in the nest on the level of care expressed as an adult. I also tested if differences in problem-solving ability were related to differences in parental care behavior. Although I found that problem-solving parents fledged more offspring than parents that could not solve the problem, parental care was not associated with any measure of problem-solving ability. Finally, I found that individual variation in parental care reaction norms predicted the growth rate, size, and immune response of nestlings, which in turn positively affected offspring survival and recruitment. My findings reveal factors maintaining individual differences in parental care behavior and offer new insights into the causes and consequences of individual variation.

Parental care is likely to evolve when benefits of care are greater than costs. Provision of parental care may buffer vulnerable offspring against unpredictable or hazardous environments permitting parents to breed in situations too hostile for unassisted juvenile survival. The nature of environmental unpredictability faced by parents and their offspring (e.g., availability of nutritional resources, breeding resources and/or the strength of competition) provides the ecological context in which costs and benefits of parental traits are defined. Therefore investigations about how the environment might shape parental traits ought not only to be conducted in the laboratory but also in a natural setting where unanticipated parameters may have profound effects on theoretical predictions. I conducted a series of manipulative experiments and observational studies in the laboratory and in the field using burying beetles, Nicrophorus vespilloides, to examine the effects of environmental variation on parental competitive ability, reproductive productivity, longevity and the expression of parental sex-role differences and alternative reproductive tactics. In these beetles a relative size advantage confers success in contests for scarce and vital breeding resources so a central prediction was that reproductive success would be positively correlated with body size. In contrast I found that reproductive performance was favoured over contest success when nutritional resources were delayed temporarily during a developmental window. Larger beetles do win contests for breeding-resources but the benefits of being large depend on the quality of the social environment experienced (i.e., the relative size of an opponent). In a naturalistic setting, smaller males avoided direct contests because they attracted proportionately more females and as a result their breeding associations were more often monogamous. This has potential benefits for females because they avoid female-female contests and brood parasitism. Variation in the nutritional environment provided by parents (the carcass size on which offspring are reared) directly influences body size creating a dynamism between the nutritional and social environments experienced by these beetles depending on their size, which has ramifications for their individual success and maintenance of alternative strategies in the population as a whole.

Parental care is one of the most successful strategies for providing offspring survival. There are differences in type of care between taxa. There are biparental care, maternal care, paternal care and alloparental care. Bees of the genus Ceratina are suitable model taxon for study of parental care evolution. There is a long time known maternal care and eusociality, in this genus. A species of the genus Ceratina, which has biparental care, is introduced in this thesis. Field experiments were performed from 2011 to 2013 in Podyjí National Park, especially in locality Havraníky heath. Four model species, which are occurring in the Czech Republic, were selected: C. chalybea, C. cucurbitina, C. cyanea and C. nigrolabiata. Artificial nesting opportunities were installed to the field site. Relationship between individuals in nests of C. nigrolabiata was examined by newly developed microsatellite loci. All studied species are solitary in nesting behavior. Their nest structure and nesting phenology is described. Guarding of full brood nest to adulthood of offspring is characteristic behavioral trait for Ceratina bees. This guarding is essential for offspring survival. Experimental nests with removed mother often failed by ant predation, parasitation by chalcid wasp and nest usurpation by other individuals of the...

Sexual conflict, the different interests of males and females over reproduction, is a potent evolutionary force. Here I investigate sexual conflict in the context of parental care by focussing on two questions: (i) which behavioural, morphological and environmental traits influence the parents’ decision to care for the brood or desert? (ii) How does sexual conflict influence the evolution of behaviour and morphology? I investigate both questions using a small, polygamous passerine bird, the Eurasian penduline tit Remiz pendulinus, which exhibits intense sexual conflict over parental care such that either the male, the female or both parents desert the clutch. Using detailed behavioural observations during the crucial few days preceding desertion, I argue that it may be in the parents’ best interest to conceal their intention to care for (or desert) their brood. The rapid resulting process that leads to variable parental care resembles a coordination game in which either parent may desert first. I developed a game-theoretical model that suggests that a key to resolving the conflict between parents is the sex difference in reproductive payoffs for given parental care strategies, rather than differences in parental quality per se. Environmental variables (e.g. food availability and mating opportunities) seem only subsidiary in the decision-making process of parents. My final chapter explores ramifications of sexual conflict at an evolutionary timescale. By comparing the highly polygamous Eurasian penduline tit with the monogamous Cape penduline tit, I show that morphological and behavioural differences between these two species are consistent with predictions of sexual conflict theory. During my PhD I also identified that there is considerable variation in breeding systems within different species of penduline tits. I argue that by studying these systems new insights will emerge into (i) the drivers of breeding systems, and (ii) neural and genomic traits that underlie breeding system evolution.

Orientador: Eliane Gonçalves de Freitas / Banca: Gilson Luiz Volpato / Banca: Regina Helena Ferraz Macedo / Resumo: O comportamento reprodutivo dos ciclídeos envolve diferentes sistemas de acasalamento e cuidado parental. No entanto, as espécies neotropicais são pouco conhecidas em relação às africanas. A maior parte dos ciclídeos neotropicais exibe cuidado biparental com predomínio da monogamia (diferentemente dos ciclídeos africanos cujo cuidado intrabucal uniparental prevalece). Laetacara sp. é uma nova espécie de ciclídeo sul-americano encontrada em abundância em riachos bastante degradados. A ocupação desses ambientes pode ser favorecida pelas estratégias reprodutivas da espécie. Assim, neste estudo descrevemos o comportamento reprodutivo de Laetacara sp. para explorarmos sua importância na determinação do sucesso dessa espécie em ambientes degradados. Inicialmente, descrevemos as fases e as unidades do comportamento reprodutivo (Capítulo 1). Em seguida, quantificamos a cooperação entre machos e fêmeas ao longo do ciclo reprodutivo (Capítulo 2). O comportamento reprodutivo de Laetacara sp. é iniciado com a defesa territorial pelo macho e envolve a formação do casal, construção de ninho, acasalamento e cuidado biparental dos ovos e larvas no substrato. O cuidado parental foi dividido em Manutenção (ventilação e limpeza dos ovos e larvas) e Defesa (interações agressivas contra intrusos nas fases estacionárias e livre natante). Na fase pré-acasalamento, os machos investiram mais em defesa territorial, enquanto as fêmeas investiram mais em construção de ninhos. Na fase ovo/larva, as fêmeas permaneceram mais tempo próximas à prole do que os machos, sem diferir na fase seguinte. Porém, os pais permaneceram por mais tempo junto à prole natante, indicando que nessa fase os filhotes são mais vulneráveis. O comportamento reprodutivo de Laetacara sp. parece ser uma das adaptações para a sobrevivência em ambientes aquáticos degradados...(Resumo completo, clicar acesso eletrônico abaixo) / Abstract: The reproductive behaviour of cichlid fishes attracts many researchers because it is expressed through different types of mating systems and parental care. However, neotropical species are still little studied, in comparison to African species. Most Neotropical cichlids are monogamous and biparental care prevails (contrary to African cichlids where mouth brooding and uniparental care are the rule). Laetacara sp. is a new South American cichlid mainly found in degraded streams. Species occupation of such environments may be facilited by reproductive strategies. Thus, the aim of this study was to describe the reproductive behaviour of Laetacara sp. to evaluate its daptative value for living successfully in degraded environments. In a first step, the phases and units of reproductive behaviour were described (Chapter 1). In a second step, cooperation between males and females during reproductive cycle was quantified (Chapter 2). Reproductive behaviour of Laetacara sp. started with territorial defense by males and involved pair bonding, nest building, mating and biparental care of eggs and wrigglers on the substrate. Parental care was divided into Nurturance (fanning and cleaning eggs and wrigglers) and Defense (aggressive contests against intruders in the brood stationary and free-swimming phases). In the pre-spawning stage, males invest more in territory defense while females invest more in nest building. In the egg/larva phase, females remains close to the brood more than males, but time spent near the brood was similar for both parents in the free-swimming phase and higher than in the previous phase, which indicates higher vulnerability of the fry. Reproductive behaviour of Laetacara sp. should be one of several adaptations that enhances the chance of surviving in aquatic degraded environments. This occurs, in part because this species can to build nests in sandy ...(Complete abstract click electronic access below) / Mestre