Keyne Monro

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.

Light quantity and quality induce shade-avoiding plasticity in a marine macroalga

Light‐induced plasticity in plant morphology is considered adaptive in terrestrial habitats that vary in light, but remains unexplored for marine habitats. This is despite similar modes of growth, development and photosynthetic equipment in terrestrial and marine photoautotrophs and similarly dynamic light environments. We tested whether manipulations of light quantity and quality induce morphological plasticity in the marine macroalga, Asparagopsis armata. Using multivariate analyses (principal components analyses and multivariate analyses of covariance), we show that correlated morphological traits underlie a fundamental growth strategy characterized by the production of phalanx and guerrilla phenotypes in environments that mimic light and shade respectively. This foraging response is not under simple genetic or environmental control, but influenced by interactions between genotype and environment. Evidence of plasticity and genetic variation in plasticity in a marine modular organism generates additional, testable hypotheses on the ecological consequences of variation in growth form that may further explain the evolution of plasticity.

Fitness consequences of larval traits persist across the metamorphic boundary

Metamorphosis is thought to provide an adaptive decoupling between traits specialized for each life‐history stage in species with complex life cycles. However, an increasing number of studies are finding that larval traits can carry‐over to influence postmetamorphic performance, suggesting that these life‐history stages may not be free to evolve independently of each other. We used a phenotypic selection framework to compare the relative and interactive effects of larval size, time to hatching, and time to settlement on postmetamorphic survival and growth in a marine invertebrate, Styela plicata. Time to hatching was the only larval trait found to be under directional selection, individuals that took more time to hatch into larvae survived better after metamorphosis but grew more slowly. Nonlinear selection was found to act on multivariate trait combinations, once again acting in opposite directions for selection acting via survival and growth. Individuals with above average values of larval traits were most likely to survive, but surviving individuals with intermediate larval traits grew to the largest size. These results demonstrate that larval traits can have multiple, complex fitness consequences that persist across the metamorphic boundary; and thus postmetamorphic selection pressures may constrain the evolution of larval traits.

The adaptive value of functional and life-history traits across fertility treatments in an annual plant

BACKGROUND AND AIMS Plant functional traits are assumed to be adaptive. As selection acts on individuals and not on traits, interpreting the adaptive value of a trait not may be straightforward. For example, productive leaves are associated with fertile environments. However, it is not clear if productive leaves confer an advantage in these habitats, or if they are an advantage as part of a suite of coordinated traits. METHODS Genotypes of Arabidopsis thaliana were grown in high and low nutrient treatments and low, neutral and high pH treatments. Nutrient availability is reduced in acidic or basic soils relative to neutral pH soils. pH treatments were used to alter the availability of resources rather than the amount of resources. KEY RESULTS Leaf function (specific leaf area, SLA) and life history (size at reproduction, age at reproduction) were variable across genotypes and were plastic. High nutrient availability induced higher SLA and larger size at reproduction. Genotypes that reproduced at large size in high nutrient conditions at neutral pH had the greatest fruit production. SLA was only indirectly related to fruit production through a causal relationship with rosette size; in high nutrient conditions, plants with high SLA were large at reproduction and had higher fruit production. In high nutrient and high pH treatments, plants were large at reproduction, but large size at reproduction was associated with low fecundity. This suggests that large size is adaptive under high nutrient availability. CONCLUSIONS Interpreting the adaptive value of functional traits will sometimes only be possible when these traits are considered as a suite of correlated and coordinated traits. Leaf functional traits may be important in defining adaptive strategies in A. thaliana but only through how they affect plant life history. Finally, manipulating soil pH can be a valuable tool in assessing adaptive plasticity on nutrient gradients.

The maintenance of sperm variability: context-dependent selection on sperm morphology in a broadcast spawning invertebrate.

Why are sperm so variable despite having a singular, critical function and an intimate relationship with fitness? A key to understanding the evolution of sperm morphology is identifying which traits enable sperm to be successful fertilizers. Several sperm traits (e.g., tail length, overall size) are implicated in sperm performance, but the benefits of these traits are likely to be highly context dependent. Here, we examined phenotypic selection on sperm morphology of a broadcast spawning tube worm (Galeolaria gemineoa). We conducted laboratory experiments to measure the relationship between average sperm morphology and relative fertilization success across a range of sperm environments that were designed to approximate the range of sperm concentrations and ages encountered by eggs in nature. We found that the strength and form of multivariate selection varied substantially across our environmental gradients. Sperm with long tails and small heads were favored in high‐concentration environments, whereas sperm with long heads were favored at low concentrations and old ages. We suggest variation in the local fertilization environment and resulting differences in selection can preserve variability in sperm morphology both within and among males.

Selection in Modular Organisms: Is Intraclonal Variation in Macroalgae Evolutionarily Important?

Theoretical and practical difficulties occur when defining the units of selection in modular organisms that grow by iteration of repeated parts (modules). Modules may become physically autonomous through fragmentation and may vary because of genetic variation arising in somatic cell lineages. Since cells destined for gamete production are not sequestered in early development, heritable variation and selection among asexual progeny are possible. We used the branching red macroalgae Delisea pulchra and Asparagopsis armata to test whether modules fulfill three fundamental criteria for units of selection: that they replicate, that they display heritable variation, and that selective agents distinguish among the variants. We detected significant phenotypic variation among modules for fitness‐related traits (growth, secondary metabolite concentrations, and rates of tissue loss to herbivory) in each species and significant heritability estimates for secondary metabolite production and tissue loss to herbivory in D. pulchra. Variation in growth rate among A. armata modules was largely phenotypic with small but important estimates of genetic variation. Our results indicate that selection may indeed act on phenotypic variation among modules within individuals and that this process may effect evolutionary change within asexual lineages given sufficient genetic variation in the traits examined.

Transgenerational plasticity and environmental stress: do paternal effects act as a conduit or a buffer?

Summary For most organisms, early life-history stages are the most sensitive to environmental stress and so transgenerational phenotypic plasticity, whereby the parental environment and offspring environment interact to alter the phenotype of the offspring, is viewed as key to promoting persistence in the face of environmental change. While there has been long-standing interest in the role of transgenerational plasticity via the maternal line (traditionally the field of maternal effects), increasingly it appears that paternal effects can also play a role. Despite the emerging role of paternal effects in studies of global change, key knowledge gaps remain: first, whether paternal effects act to increase or decrease offspring performance remains largely unexplored; second, the relative roles of maternal and paternal effects are rarely disentangled; and third, the role of environmental variation, a key determinant of the benefits of transgenerational plasticity, has not been explored with regard to paternal effects. Here, we explore all three issues using the marine tubeworm Galeolaria caespitosa, an important habitat-forming species in southern Australia. We found that both paternal and maternal experiences affected key stages of offspring performance (fertilization and larval development) and, surprisingly, paternal effects were often stronger than maternal effects. Furthermore, we found that paternal effects often reduced offspring performance, especially when environments varied compared with when environments were stable. Our results suggest that, while transgenerational plasticity may play an important role in modifying the impacts of global change, these effects are not uniformly positive. Importantly, paternal effects can be as strong, or stronger, than maternal effects and environmental variability strongly alters the impacts of paternal effects.

The Potential for Evolutionary Responses to Cell-Lineage Selection on Growth Form and Its Plasticity in a Red Seaweed

Despite much theoretical discussion on the evolutionary significance of intraclonal genetic variation, particularly for modular organisms whose lack of germ‐soma segregation allows for variants arising in clonal growth to contribute to evolutionary change, the potential of this variation to fuel adaptation remains surprisingly untested. Given intraclonal variation, mitotic cell lineages, rather than sexual offspring, may frequently act as units of selection. Here, we applied artificial selection to such lineages in the branching red seaweed Asparagopsis armata, targeting aspects of clonal growth form and growth‐form plasticity that enhance light acquisition on patchy subtidal reefs and predicting that a genetic basis to intraclonal variation may promote significant responses that cannot accompany phenotypic variation alone. Cell‐lineage selection increased variation in branch proliferation among A. armata genets and successfully altered its plasticity to light. Correlated responses in the plasticity of branch elongation, moreover, showed that cell‐lineage selection may be transmitted among the plasticities of growth‐form traits in A. armata via pleiotropy. By demonstrating significant responses to cell‐lineage selection on growth‐form plasticity in this seaweed, our study lends support to the notion that intraclonal genetic variation may potentially help clonal organisms to evolve adaptively in the absence of sex and thereby prove surprisingly resilient to environmental change.

INTERSPECIFIC COMPETITION ALTERS NONLINEAR SELECTION ON OFFSPRING SIZE IN THE FIELD

Offspring size is one of the most important life‐history traits with consequences for both the ecology and evolution of most organisms. Surprisingly, formal estimates of selection on offspring size are rare, and the degree to which selection (particularly nonlinear selection) varies among environments remains poorly explored. We estimate linear and nonlinear selection on offspring size, module size, and senescence rate for a sessile marine invertebrate in the field under three different intensities of interspecific competition. The intensity of competition strongly modified the strength and form of selection acting on offspring size. We found evidence for differences in nonlinear selection across the three environments. Our results suggest that the fitness returns of a given offspring size depend simultaneously on their environmental context, and on the context of other offspring traits. Offspring size effects can be more pervasive with regards to their influence on the fitness returns of other traits than previously recognized, and we suggest that the evolution of offspring size cannot be understood in isolation from other traits. Overall, variability in the form and strength of selection on offspring size in nature may reduce the efficacy of selection on offspring size and maintain variation in this trait.