Dustin J. Marshall

Projecting coral reef futures under global warming and ocean acidification

Many physiological responses in present-day coral reefs to climate change are interpreted as consistent with the imminent disappearance of modern reefs globally because of annual mass bleaching events, carbonate dissolution, and insufficient time for substantial evolutionary responses. Emerging evidence for variability in the coral calcification response to acidification, geographical variation in bleaching susceptibility and recovery, responses to past climate change, and potential rates of adaptation to rapid warming supports an alternative scenario in which reef degradation occurs with greater temporal and spatial heterogeneity than current projections suggest. Reducing uncertainty in projecting coral reef futures requires improved understanding of past responses to rapid climate change; physiological responses to interacting factors, such as temperature, acidification, and nutrients; and the costs and constraints imposed by acclimation and adaptation.

Offspring size plasticity in response to intraspecific competition: An adaptive maternal effect across life-history stages

When provisioning offspring, mothers balance the benefits of producing a few large, fitter offspring with the costs of decreased fecundity. The optimal balance between offspring size and fecundity depends on the environment. Theory predicts that larger offspring have advantages in adverse conditions, but in favorable conditions size is less important. Thus, if environmental quality varies, selection should favor mothers that adaptively allocate resources in response to local conditions to maximize maternal fitness. In the bryozoan Bugula neritina, we show that the intensity of intraspecific competition dramatically changes the offspring size/performance relationship in the field. In benign or extremely competitive environments, offspring size is less important, but at intermediate levels of competition, colonies from larger larvae have higher performance than colonies from smaller larvae. We predicted mothers should produce larger offspring when intermediate competition is likely and tested these expectations in the field by manipulating the density of brood colonies. Our findings matched expectations: mothers produced larger larvae at high densities and smaller larvae at low densities. In addition, mothers from high‐density environments produced larvae that have higher dispersal potential, which may enable offspring to escape crowded environments. It appears mothers can adaptively adjust offspring size to maximize maternal fitness, altering the offspring phenotype across multiple life‐history stages.

Predicting evolutionary responses to climate change in the sea.

An increasing number of short-term experimental studies show significant effects of projected ocean warming and ocean acidification on the performance on marine organisms. Yet, it remains unclear if we can reliably predict the impact of climate change on marine populations and ecosystems, because we lack sufficient understanding of the capacity for marine organisms to adapt to rapid climate change. In this review, we emphasise why an evolutionary perspective is crucial to understanding climate change impacts in the sea and examine the approaches that may be useful for addressing this challenge. We first consider what the geological record and present-day analogues of future climate conditions can tell us about the potential for adaptation to climate change. We also examine evidence that phenotypic plasticity may assist marine species to persist in a rapidly changing climate. We then outline the various experimental approaches that can be used to estimate evolutionary potential, focusing on molecular tools, quantitative genetics, and experimental evolution, and we describe the benefits of combining different approaches to gain a deeper understanding of evolutionary potential. Our goal is to provide a platform for future research addressing the evolutionary potential for marine organisms to cope with climate change.

Phenotype–environment mismatches reduce connectivity in the sea

The connectivity of marine populations is often surprisingly lower than predicted by the dispersal capabilities of propagules alone. Estimates of connectivity, moreover, do not always scale with distance and are sometimes counterintuitive. Population connectivity requires more than just the simple exchange of settlers among populations: it also requires the successful establishment and reproduction of exogenous colonizers. Marine organisms often disperse over large spatial scales, encountering very different environments and suffering extremely high levels of post-colonization mortality. Given the growing evidence that such selection pressures often vary over spatial scales that are much smaller than those of dispersal, we argue that selection will bias survival against exogenous colonizers. We call this selection against exogenous colonizers a phenotype-environment mismatch and argue that phenotype-environment mismatches represent an important barrier to connectivity in the sea. Crucially, these mismatches may operate independently of distance and thereby have the potential to explain the counterintuitive patterns of connectivity often seen in marine environments. We discuss how such mismatches might alter our understanding and management of marine populations.

The Evolutionary Ecology of Offspring Size in Marine Invertebrates

Intraspecific variation in offspring size is of fundamental ecological and evolutionary importance. The level of provisioning an organism receives from its mother can have far reaching consequences for subsequent survival and performance. In marine systems, the traditional focus was on the remarkable variation in offspring size among species but there is increasing focus on variation in offspring size within species. Here we review the incidence and consequences of intraspecific offspring-size variation for marine invertebrates. Offspring size is remarkably variable within and among marine invertebrate populations. We examined patterns of variation in offspring size within populations using a meta-analysis of the available data for 102 species across 7 phyla. The average coefficient of variation in offspring size within populations is 9%, while some groups (e.g., direct developers) showed much more variation (15%), reflecting a fourfold difference between the largest and smallest offspring in any population. Offspring-size variation can have for reaching consequences. Offspring size affects every stage of a marine invertebrates life history, even in species in which maternal provisioning accounts for only a small proportion of larval nutrition (i.e., planktotrophs). In species with external fertilization, larger eggs are larger targets for sperm and as such, the sperm environment may select for different egg sizes although debate continues over the evolutionary importance of such effects. Offspring size affects the planktonic period in many species with planktotrophic and lecithotrophic development, but we found that this effect is not universal. Indeed, much of the evidence for the effects of offspring size on the planktonic period is limited to the echinoids and in this group and other taxa there is variable evidence, suggesting further work is necessary. Post-metamorphic effects of offspring size were strong in species with non-feeding larvae and direct development: bigger offspring generally have higher post-metamorphic survival, higher growth rates and sometimes greater fecundity. Although there is limited evidence for the mechanisms underlying these effects, the size of post-metamorphic feeding structures and resistance to low-food availability appear to be good candidates. There was limited evidence to assess the effects of offspring size on post-metamorphic performance in planktotrophs but surprisingly, initial indications suggest that such effects do exist and in the same direction as for species with other developmental modes. Overall, we suggest that for direct developers and species with non-feeding larvae, the post-metamorphic effects of offspring size will be greatest source of selection. Offspring-size variation can arise through a variety of sources, both within and among populations. Stress, maternal size and nutrition, and habitat quality all appear to be major factors affecting the size of offspring, but more work on sources of variation is necessary. While theoretical considerations of offspring size can now account for variation in offspring size among mothers, they struggle to account for within-brood variation. We suggest alternative approaches such as game theoretic models that may be useful for reconciling within-clutch variation. While some of the first theoretical considerations of offspring size were based on marine invertebrates, many of the assumptions of these models have not been tested, and we highlight some of the important gaps in understanding offspring-size effects. We also discuss the advantages of using offspring size as a proxy for maternal investment and review the evidence used to justify this step. Overall, offspring size is likely to be an important source of variation in the recruitment of marine invertebrates. The quality of offspring entering a population could be as important as the quantity and further work on the ecological role of offspring size is necessary. From an evolutionary standpoint, theoretical models that consider every life-history stage, together with the collection of more data on the relationship between offspring size and performance at each stage, should bring us closer to understanding the evolution of such a wide array of offspring sizes and developmental modes among species.

Coping with environmental uncertainty: dynamic bet hedging as a maternal effect

Mothers in a range of taxa manipulate the phenotype of their offspring in response to environmental change in order to maximize their own fitness. Most studies have focused on changes in the mean phenotype of offspring. Focusing on mean offspring phenotypes is appropriate for species in which mothers are likely to successfully predict the environment their offspring will experience, but what happens when the offsprings environment is unpredictable? Theory suggests that when mothers face uncertainty regarding their offsprings environment, they should increase within-clutch variation in the offspring phenotype (i.e. they should bet hedge). While comparative analyses support the idea that mothers do bet hedge in response to environmental unpredictability, empirical tests are very rare and it remains unclear whether mothers adaptively adjust variance in offspring traits (a phenomenon we call dynamic bet hedging). As a first step towards examining dynamic bet hedging, we reanalysed data from five previously published studies. These studies were across a range of taxa, but all manipulated the maternal environment/phenotype and then examined changes in mean offspring size. We found some support for the theoretical predictions that mothers should increase within-clutch offspring size variation when faced with unpredictable environments. We predict that dynamic bet hedging is more common than previously anticipated and suggest that it has some interesting implications for the studies that focus on shifts in mean offspring traits alone. Hence, future studies should examine maternal effects on both the mean and the variance of offspring traits.

OFFSPRING SIZE AFFECTS THE POST-METAMORPHIC PERFORMANCE OF A COLONIAL MARINE INVERTEBRATE

The positive relationship between offspring size and offspring fitness is a fundamental assumption of life-history theory, but it has received relatively little attention in the marine environment. This is surprising given that substantial intraspecific variation in offspring size is common in marine organisms and there are clear links between larval experience and adult performance. The metamorphosis of most marine invertebrates does not represent a newbeginning, and larval experiences can have effects that carry over to juvenile survival and growth. We show that larval size can have equally important carryover effects in a colonial marine invertebrate. In the bryozoan Bugula neritina, the size of the non-feeding larvae has a prolonged effect on colony performance after metamorphosis. Colonies that came from larger larvae survived better, grew faster, and reproduced sooner or produced more embryos than colonies that came from smaller larvae. These effects crossed generations, with colonies from larger larvae themselves producing larger larvae. These effects were found in two populations (in Australia and in the United States) in contrasting habitats.

MALE-BY-FEMALE INTERACTIONS INFLUENCE FERTILIZATION SUCCESS AND MEDIATE THE BENEFITS OF POLYANDRY IN THE SEA URCHIN HELIOCIDARIS ERYTHROGRAMMA

Abstract Numerous studies have reported that females benefit from mating with multiple males (polyandry) by minimizing the probability of fertilization by genetically incompatible sperm. Few, however, have directly attributed variation in female reproductive success to the fertilizing capacity of sperm. In this study we report on two experiments that investigated the benefits of polyandry and the interacting effects of males and females at fertilization in the free-spawning Australian sea urchin Heliocidaris erythrogramma. In the first experiment we used a paired (split clutch) experimental design and compared fertilization rates within female egg clutches under polyandry (eggs exposed to the sperm from two males simultaneously) and monandry (eggs from the same female exposed to sperm from each of the same two males separately). Our analysis revealed a significant fertilization benefit of polyandry and strong interacting effects of males and females at fertilization. Further analysis of these data strongly suggested that the higher rates of fertilization in the polyandry treatment were due to an overrepresentation of fertilizations due to the most compatible male. To further explore the interacting effects of males and females at fertilization we performed a second factorial experiment in which four males were crossed with two females (in all eight combinations). In addition to confirming that fertilization success is influenced by male × female interactions, this latter experiment revealed that both sexes contributed significant variance to the observed patterns of fertilization. Taken together, these findings highlight the importance of male × female interactions at fertilization and suggest that polyandry will enable females to reduce the cost of fertilization by incompatible gametes.

OFFSPRING SIZE EFFECTS MEDIATE COMPETITIVE INTERACTIONS IN A COLONIAL MARINE INVERTEBRATE

Over the past 30 years, numerous attempts to understand the relationship between offspring size and fitness have been made, and it has become clear that this critical relationship is strongly affected by environmental heterogeneity. For marine invertebrates, there has been a long-standing interest in the evolution of offspring size, but there have been very few empirical and theoretical examinations of post-metamorphic offspring size effects, and almost none have considered the effect of environmental heterogeneity on the offspring size/fitness relationship. We investigated the post-metamorphic effects of offspring size in the field for the colonial marine invertebrate Botrylloides violaceus. We also examined how the relationship between offspring size and performance was affected by three different types of intraspecific competition. We found strong and persistent effects of offspring size on survival and growth, but these effects depended on the level and type of intraspecific competition. Generally, competition strengthened the advantages of increasing maternal investment. Interestingly, we found that offspring size determined the outcome of competitive interaction: juveniles that had more maternal investment were more likely to encroach on another juveniles territory. This suggests that mothers have the previously unrecognized potential to influence the outcome of competitive interactions in benthic marine invertebrates. We created a simple optimality model, which utilized the data generated from our field experiments, and found that increasing intraspecific competition resulted in an increase in predicted optimal size. Our results suggest that the relationship between offspring size and fitness is highly variable in the marine environment and strongly dependent on the density of conspecifics.

TRANSGENERATIONAL PLASTICITY IN THE SEA : CONTEXT-DEPENDENT MATERNAL EFFECTS ACROSS THE LIFE HISTORY

Maternal effects can have dramatic influences on the phenotype of offspring. Maternal effects can act as a conduit by which the maternal environment negatively affects offspring fitness, but they can also buffer offspring from environmental change by altering the phenotype of offspring according to local environmental conditions and as such, are a form of transgenerational plasticity. The benefits of maternal effects can be highly context dependent, increasing performance in one life-history stage but reducing it in another. While maternal effects are increasingly well understood in terrestrial systems, studies in the marine environment are typically restricted to a single, early life-history stage. Here, I examine the role of maternal effects across the life history of the bryozoan Bugula neritina. I exposed maternal colonies to a common pollution stress (copper) in the laboratory and then placed them in the field for one week to brood offspring. I then examined the resistance of offspring to copper from toxicant-exposed and toxicant-naïve mothers and found that offspring from toxicant-exposed mothers were larger, more dispersive, and more resistant to copper stress than offspring from naïve mothers. However, maternal exposure history had pervasive, negative effects on the post-metamorphic performance (particularly survival) of offspring: offspring from toxicant-exposed mothers had poorer performance after six weeks in the field, especially when facing high levels of intraspecific competition. Maternal experience can have complex effects on offspring phenotype, enhancing performance in one life-history stage while decreasing performance in another. The context-dependent costs and benefits associated with maternally derived pollution resistance may account for why such resistance is induced rather than continually expressed: mothers must balance the benefits of producing pollution-resistant larvae with the costs of producing poorer performing adults (in the absence of pollution).