Causes of adaptive differences in age-dependent reproductive effort

Sexually selected ornaments are among the most spectacular traits in nature. Indeed, the extreme costs associated with producing sexual traits seem to play a crucial role in their evolution by enforcing honest levels of advertisement: only males with high levels of acquired resources (or high ‘condition’, as it is known in the literature) can afford to produce extravagant signals, a phenomenon which maintains signal reliability in a constant environment. In my thesis I examine many implications of this condition-dependent model of ornament and preference evolution for variation in age-dependent allocation to sexual signals and other life history traits. In Chapter 1, I review theoretical implications of condition-dependent signalling for life history and sexual selection theory. I note that a universal cost of expenditure in sexual advertisement is metabolic in nature: metabolites used to fund ornament expression are by definition unavailable to other life history traits that compete for a limited resource pool. This universal constraint on expenditure does more than maintain honesty (as noted above), however: the reliance of sexual displays on high levels of nutrient acquisition may help maintain genetic variation in sexual signals that would otherwise be eroded by strong mate choice, and without which the selective basis for good-genes choice would disappear. Three mechanisms in particular probably help to maintain genetic variation in acquisition. 1) Because acquiring resources and converting them efficiently to useful forms depends on the high function of many biochemical pathways, condition is undoubtedly highly polygenic, which slows the erosion of genetic variation under strong directional selection by females (especially in the presence of epistatic interactions). 2) The highly polygenic nature of condition also presents a large target for mutation, which continually restores variation at the loci under selection. 3) The many loci underlying condition may also be particularly sensitive to environmental heterogeneity in time or space. By favouring the most ornate males, females acquire high performing genes for their offspring, regardless of the precise allele combinations that have conferred the ability to acquire resources. Selection on specific alleles is liable to fluctuate over time or space whenever allelic performance is strongly context-specific. I close by noting the considerable challenges in advancing research on sexual selection and life history allocation, including the fact that two key processes central to life history (acquisition and allocation) are latent variables that interact in complexways and are intrinsically difficult to measure empirically. In the remainder of my thesis I conduct a series of experiments involving decorated crickets, Gryllodes sigillatus, which are useful models for studying life history because they enable precise measurement of male reproductive effort. Male G. sigillatus face important allocation decisions owing to the highly polyandrous nature of females, and the substantial costs involved in signalling and mating. Chapter 2 examines sex differences in age-dependent reproductive effort as a function of diet and development stage. I reared outbred crickets using four combinations of diet nutritional quality, and studied the effects of these combinations on male and female reproductive effort (calling effort in males and fecundity in females) and longevity. While I expected males to be more sensitive than females to variation in diet and developmental changes in its quality, I actually observed the opposite: males in all treatments increased calling effort over time, exhibiting consistently positive covariance between calling effort and longevity across treatments. By contrast, the relationships between female reproductive effort and longevity changed dramatically across treatments, and females who lived to intermediate ages had the highest fecundity. Although my results support sex-specific selection on life history allocation over time, a compelling additional explanation for my findings relates to the strategic role of calling for achieving male fitness. In the absence of positive feedback from potential mates, perhaps male allocation to sexual advertisement is careful and only increases gradually as a function of accumulating metabolic resources and increasing risk of intrinsic mortality. Alleles underlying condition are expected to be particularly sensitive to environmental heterogeneity. While this sensitivity may help maintain additive variation in male quality (which is essential for the sustenance of adaptive good-genes mate choice, as noted in Chapter 1), too much environmental sensitivity could also underiii mine the signal value of the male trait. For example, if there are strong genotypeby- environment interactions (GEIs) for sexual advertisement, in a rapidly changing environment females risk favouring a male whose alleles are no longer best suited to current conditions. This problem is particularly pressing for animals like crickets where males exhibit a behaviourally plastic sexual display (such as calling), and so may dynamically adjust signalling effort over time. In Chapter 3, I used inbred lines of decorated crickets to quantify age and diet dependent genetic variation in male signalling. I demonstrate that while genetic correlations across diets were quite strong for morphological traits, correlations between measures of the male sexual trait rapidly approached zero as I increased the distance in time (i.e., across widely spaced ages) or diet (i.e., comparing more dissimilar dietary histories) between samples. While extrapolating from my laboratory experiments to nature is difficult, my findings nevertheless cast doubt on the value of behaviourally dynamic signals (such as cricket calls) for reliably indicating genetic quality in realistically complex environments. In Chapter 4 I used physiological assays to evaluate factors affecting metabolite storage and use over time in decorated crickets. I manipulated the acquisition ability of all males using artificial diets that varied linearly in nutrient quality, and manipulated access to female mates over the course of the second week of adult life. By sacrificing crickets at key stages before and after manipulating the diet and social environment, I was able to estimate changes in stored metabolites, and relate these changes to calling effort and longevity. During the first week of adulthood (in the absence of females), higher diet quality significantly increased calling effort and storage of lipid, glycogen, and carbohydrate (but not protein). The presence of females increased both the probability of calling and the amount of calling during the second week, whereas diet quality only improved calling effort. By the end of the second week, calling effort had decreased, even by high quality males in the presence of females, suggesting a depletion of resources. Furthermore, the loss of condition during week 2 covaried with calling effort during the previous week irrespective of diet. Males who started the second week in high condition lost more glycogen and carbohydrate than rivals; meanwhile, lipid accumulation covaried positively with calling effort during week 2. The contrasting patterns of storage and use for lipids compared to the ‘quick-release’ metabolites (glycogen and carbohydrates) affirms starkly distinct functions for the different storage components, and underlines the importance of specific physiological measures in life history research. Finally, in the general discussion, I attempt to synthesise my thesis’s contributions to the study of life history trade-offs involving behavioural sexual displays. I argue that my work may have strong implications for the general honesty of male advertisements, and invite further research focused on quantifying interactions between the genotype, age, and environment in natural systems. I also question the prevalence of adaptive age-dependent plasticity in sexual advertisement, arguing for the parsimony of a more mechanistic and non-adaptive explanation for variation among populations and taxa in age-dependent signalling: males vary in signalling effort primarily as a function of constraints on energy expenditure, rather than because they are carefully saving resources for future use

Exploiting animal personality to reduce chronic stress in captive fish populations

Chronic stress is a major source of welfare problems in many captive populations, including fishes. While we have long known that chronic stress effects arise from maladaptive expression of acute stress response pathways, predicting where and when problems will arise is difficult. Here we highlight how insights from animal personality research could be useful in this regard. Since behavior is the first line of organismal defense when challenged by a stressor, assays of shy-bold type personality variation can provide information about individual stress response that is expected to predict susceptibility to chronic stress. Moreover, recent demonstrations that among-individual differences in stress-related physiology and behaviors are underpinned by genetic factors means that selection on behavioral biomarkers could offer a route to genetic improvement of welfare outcomes in captive fish stocks. Here we review the evidence in support of this proposition, identify remaining empirical gaps in our understanding, and set out appropriate criteria to guide development of biomarkers. The article is largely prospective: fundamental research into fish personality shows how behavioral biomarkers could be used to achieve welfare gains in captive fish populations. However, translating potential to actual gains will require an interdisciplinary approach that integrates the expertise and viewpoints of researchers working across animal behavior, genetics, and welfare science

Exploiting animal personality to reduce chronic stress in captive fish populations

Chronic stress is a major source of welfare problems in many captive populations, including fishes. While we have long known that chronic stress effects arise from maladaptive expression of acute stress response pathways, predicting where and when problems will arise is difficult. Here we highlight how insights from animal personality research could be useful in this regard. Since behavior is the first line of organismal defense when challenged by a stressor, assays of shy-bold type personality variation can provide information about individual stress response that is expected to predict susceptibility to chronic stress. Moreover, recent demonstrations that among-individual differences in stress-related physiology and behaviors are underpinned by genetic factors means that selection on behavioral biomarkers could offer a route to genetic improvement of welfare outcomes in captive fish stocks. Here we review the evidence in support of this proposition, identify remaining empirical gaps in our understanding, and set out appropriate criteria to guide development of biomarkers. The article is largely prospective: fundamental research into fish personality shows how behavioral biomarkers could be used to achieve welfare gains in captive fish populations. However, translating potential to actual gains will require an interdisciplinary approach that integrates the expertise and viewpoints of researchers working across animal behavior, genetics, and welfare science

Exploiting animal personality to reduce chronic stress in captive fish populations

Chronic stress is a major source of welfare problems in many captive populations, including fishes. While we have long known that chronic stress effects arise from maladaptive expression of acute stress response pathways, predicting where and when problems will arise is difficult. Here we highlight how insights from animal personality research could be useful in this regard. Since behavior is the first line of organismal defense when challenged by a stressor, assays of shy-bold type personality variation can provide information about individual stress response that is expected to predict susceptibility to chronic stress. Moreover, recent demonstrations that among-individual differences in stress-related physiology and behaviors are underpinned by genetic factors means that selection on behavioral biomarkers could offer a route to genetic improvement of welfare outcomes in captive fish stocks. Here we review the evidence in support of this proposition, identify remaining empirical gaps in our understanding, and set out appropriate criteria to guide development of biomarkers. The article is largely prospective: fundamental research into fish personality shows how behavioral biomarkers could be used to achieve welfare gains in captive fish populations. However, translating potential to actual gains will require an interdisciplinary approach that integrates the expertise and viewpoints of researchers working across animal behavior, genetics, and welfare science

Choice consequences: salinity preferences and hatchling survival in the mangrove rivulus (Kryptolebias marmoratus).

In heterogeneous environments, mobile species should occupy habitats in which their fitness is maximized. Mangrove rivulus fish inhabit mangrove ecosystems where salinities range from 0 to 65 ppt, but are most often collected from areas with salinities of ∼25 ppt. We examined the salinity preference of mangrove rivulus in a lateral salinity gradient, in the absence of predators and competitors. Fish could swim freely for 8 h throughout the gradient with chambers containing salinities ranging from 5 to 45 ppt (or 25 ppt throughout in the control). We defined preference as the salinity in which the fish spent most of their time, and also measured preference strength, latency to begin exploring the arena, and number of transitions between chambers. To determine whether these traits were repeatable, each fish experienced three trials. Mangrove rivulus spent a greater proportion of time in salinities lower (5-15 ppt) than they occupy in the wild. Significant among-individual variation in the (multivariate) behavioral phenotype emerged when animals experienced the gradient, indicating strong potential for selection to drive behavioral evolution in areas with diverse salinity microhabitats. We also showed that mangrove rivulus had a significantly greater probability of laying eggs in low salinities compared with control or high salinities. Eggs laid in lower salinities also had higher hatching success compared with those laid in higher salinities. Thus, although mangrove rivulus can tolerate a wide range of salinities, they prefer low salinities. These results raise questions about factors that prevent mangrove rivulus from occupying lower salinities in the wild, whether higher salinities impose energetic costs, and whether fitness changes as a function of salinity

Macronutrient intake and simulated infection threat independently affect life history traits of male decorated crickets.

Nutritional geometry has advanced our understanding of how macronutrients (e.g., proteins and carbohydrates) influence the expression of life history traits and their corresponding trade-offs. For example, recent work has revealed that reproduction and immune function in male decorated crickets are optimized at very different protein:carbohydrate (P:C) dietary ratios. However, it is unclear how an individual's macronutrient intake interacts with its perceived infection status to determine investment in reproduction or other key life history traits. Here, we employed a fully factorial design in which calling effort and immune function were quantified for male crickets fed either diets previously demonstrated to maximize calling effort (P:C = 1:8) or immune function (P:C = 5:1), and then administered a treatment from a spectrum of increasing infection cue intensity using heat-killed bacteria. Both diet and a simulated infection threat independently influenced the survival, immunity, and reproductive effort of males. If they called, males increased calling effort at the low infection cue dose, consistent with the terminal investment hypothesis, but interpretation of responses at the higher threat levels was hampered by the differential mortality of males across infection cue and diet treatments. A high protein, low carbohydrate diet severely reduced the health, survival, and overall fitness of male crickets. There was, however, no evidence of an interaction between diet and infection cue dose on calling effort, suggesting that the threshold for terminal investment was not contingent on diet as investigated here

Host shifts result in parallel genetic changes when viruses evolve in closely related species.

Host shifts, where a pathogen invades and establishes in a new host species, are a major source of emerging infectious diseases. They frequently occur between related host species and often rely on the pathogen evolving adaptations that increase their fitness in the novel host species. To investigate genetic changes in novel hosts, we experimentally evolved replicate lineages of an RNA virus (Drosophila C Virus) in 19 different species of Drosophilidae and deep sequenced the viral genomes. We found a strong pattern of parallel evolution, where viral lineages from the same host were genetically more similar to each other than to lineages from other host species. When we compared viruses that had evolved in different host species, we found that parallel genetic changes were more likely to occur if the two host species were closely related. This suggests that when a virus adapts to one host it might also become better adapted to closely related host species. This may explain in part why host shifts tend to occur between related species, and may mean that when a new pathogen appears in a given species, closely related species may become vulnerable to the new disease

African forest elephant movements depend on time scale and individual behavior.

The critically endangered African forest elephant (Loxodonta cyclotis) plays a vital role in maintaining the structure and composition of Afrotropical forests, but basic information is lacking regarding the drivers of elephant movement and behavior at landscape scales. We use GPS location data from 96 individuals throughout Gabon to determine how five movement behaviors vary at different scales, how they are influenced by anthropogenic and environmental covariates, and to assess evidence for behavioral syndromes-elephants which share suites of similar movement traits. Elephants show some evidence of behavioral syndromes along an 'idler' to 'explorer' axis-individuals that move more have larger home ranges and engage in more 'exploratory' movements. However, within these groups, forest elephants express remarkable inter-individual variation in movement behaviours. This variation highlights that no two elephants are the same and creates challenges for practitioners aiming to design conservation initiatives

Individual differences in spatial learning are correlated across tasks but not with stress response behaviour in guppies

Cognition is vital for carrying out behaviours required for survival and reproduction. Cognitive performance varies between species, but also between individuals within populations. While variation is a prerequisite for natural selection, selection does not act on traits in isolation. The extent to which cognitive traits covary with other aspects of phenotype (e.g. personality traits) may be important in shaping evolutionary dynamics. Here we adopted a multivariate approach to test spatial learning in male Poecilia reticulata and asked whether differences in cognitive performance are associated with (repeatable) differences in stress response behaviour. Functional links between cognitive traits and ‘stress coping style’ have been hypothesized. Furthermore, individual level studies of cognitive performance typically rely on multiple testing paradigms that may themselves be a stressor. There is a risk that variation in stress responsiveness is itself a cause of apparent, but artefactual variance in cognitive ability. Fish repeatedly experienced two spatial learning tasks (maze layouts) and an acute stress response test (open field trial). We found repeatable differences between individuals in performance within and across maze layouts. On average, performance improved with experience in the first maze, consistent with spatial learning, but not in the second. Individuals varied in the trajectory of mean performance with trial number in both mazes, suggesting they differ in ‘learning rate’. Acute stress response behaviour was repeatable but predicted neither average time to solve the maze nor learning rate. We found no support for between-individual correlation between acute stress response and cognitive performance. However, we highlight the possibility that cumulative, chronic stress effects may nevertheless cause declines in performance for some individuals (leading to lack of improvement in mean time to solve the second maze). If so, this may represent a pervasive but difficult challenge for our ability to robustly estimate learning rates in studies of animal cognition

No evidence of a cleaning mutualism between burying beetles and their phoretic mites.

Burying beetles (Nicrophorus vespilloides) breed on small vertebrate carcasses, which they shave and smear with antimicrobial exudates. Producing antimicrobials imposes a fitness cost on burying beetles, which rises with the potency of the antimicrobial defence. Burying beetles also carry phoretic mites (Poecilochirus carabi complex), which breed alongside them on the carcass. Here we test the novel hypothesis that P. carabi mites assist burying beetles in clearing the carcass of bacteria as a side-effect of grazing on the carrion. We manipulated the bacterial environment on carcasses and measured the effect on the beetle in the presence and absence of mites. With next-generation sequencing, we investigated how mites influence the bacterial communities on the carcass. We show that mites: 1) cause beetles to reduce the antibacterial activity of their exudates but 2) there are no consistent fitness benefits of breeding alongside mites. We also find that mites increase bacterial diversity and richness on the carcass, but do not reduce bacterial abundance. The current evidence does not support a cleaning mutualism between burying beetles and P. carabi mites, but more work is needed to understand the functional significance and fitness consequences for the beetle of mite-associated changes to the bacterial community on the carcass