Climate adaptation and vulnerability of foundation species in a global change hotspot.

Climate change is altering species ranges, and relative abundances within ranges, as populations become differentially adapted and vulnerable to the climates they face. Understanding present species ranges, whether species harbour and exchange adaptive variants, and how variants are distributed across landscapes undergoing rapid change, is therefore crucial to predicting responses to future climates and informing conservation strategies. Such insights are nonetheless lacking for most species of conservation concern. We assess genomic patterns of neutral variation, climate adaptation and climate vulnerability (offsets in predicted distributions of putatively adaptive variants across present and future landscapes) for sister foundation species, the marine tubeworms Galeolaria caespitosa and Galeolaria gemineoa, in a sentinel region for climate change impacts. We find that species are genetically isolated despite uncovering sympatry in their ranges, show parallel and nonparallel signals of thermal adaptation on spatial scales smaller than gene flow across their ranges, and are predicted to face different risks of maladaptation under future temperatures across their ranges. Our findings have implications for understanding local adaptation in the face of gene flow, and generate spatially explicit predictions for climatic disruption of adaptation and species distributions in coastal ecosystems that could guide experimental validation and conservation planning.

Within-population variation in body size plasticity in response to combined nutritional and thermal stress is partially independent from variation in development time.

Ongoing climate change has forced animals to face changing thermal and nutritional environments. Animals can adjust to such combinations of stressors via plasticity. Body size is a key trait influencing organismal fitness, and plasticity in this trait in response to nutritional and thermal conditions varies among genetically diverse, locally adapted populations. The standing genetic variation within a population can also influence the extent of body size plasticity. We generated near-isogenic lines from a newly collected population of Drosophila melanogaster at the mid-point of east coast Australia and assayed body size for all lines in combinations of thermal and nutritional stress. We found that isogenic lines showed distinct underlying patterns of body size plasticity in response to temperature and nutrition that were often different from the overall population response. We then tested whether plasticity in development time could explain, and therefore regulate, variation in body size to these combinations of environmental conditions. We selected five genotypes that showed the greatest variation in response to combined thermal and nutritional stress and assessed the correlation between response of developmental time and body size. While we found significant genetic variation in development time plasticity, it was a poor predictor of body size among genotypes. Our results therefore suggest that multiple developmental pathways could generate genetic variation in body size plasticity. Our study emphasizes the need to better understand genetic variation in plasticity within a population, which will help determine the potential for populations to adapt to ongoing environmental change.

Multilevel Selection on Offspring Size and the Maintenance of Variation.

AbstractMultilevel selection on offspring size occurs when offspring fitness depends on both absolute size (hard selection) and size relative to neighbors (soft selection). We examined multilevel selection on egg size at two biological scales-within clutches and among clutches from different females-using an external fertilizing tube worm. We exposed clutches of eggs to two sperm environments (limiting and saturating) and measured their fertilization success. We then modeled environmental (sperm-dependent) differences in hard and soft selection on individual eggs as well as selection on clutch-level traits (means and variances). Hard and soft selection differed in strength and form depending on sperm availability-hard selection was consistently stabilizing; soft selection was directional and favored eggs relatively larger (sperm limitation) or smaller (sperm saturation) than the clutch mean. At the clutch level, selection on mean egg size was largely concave, while selection on within-clutch variance was weak but generally negative-although some correlational selection occurred between these two traits. Importantly, we found that the optimal clutch mean egg size differed for mothers and offspring, suggesting some antagonism between the levels of selection. We thus identify several pathways that may maintain offspring size variation: environmentally (sperm-) dependent soft selection, antagonistic multilevel selection, and correlational selection on clutch means and variances. Multilevel approaches are powerful but seldom-used tools for studies of offspring size, and we encourage their future use.

Thermal performance curves reveal shifts in optima, limits and breadth in early life.

Understanding thermal performance at life stages that limit persistence is necessary to predict responses to climate change, especially for ectotherms whose fitness (survival and reproduction) depends on environmental temperature. Ectotherms often undergo stage-specific changes in size, complexity and duration that are predicted to modify thermal performance. Yet performance is mostly explored for adults, while performance at earlier stages that typically limit persistence remains poorly understood. Here, we experimentally isolate thermal performance curves at fertilization, embryo development and larval development stages in an aquatic ectotherm whose early planktonic stages (gametes, embryos and larvae) govern adult abundances and dynamics. Unlike previous studies based on short-term exposures, responses with unclear links to fitness or proxies in lieu of explicit curve descriptors (thermal optima, limits and breadth), we measured performance as successful completion of each stage after exposure throughout, and at temperatures that explicitly capture curve descriptors at all stages. Formal comparisons of descriptors using a combination of generalized linear mixed modelling and parametric bootstrapping reveal important differences among life stages. Thermal performance differs significantly from fertilization to embryo development (with thermal optimum declining by ∼2°C, thermal limits shifting inwards by ∼8-10°C and thermal breadth narrowing by ∼10°C), while performance declines independently of temperature thereafter. Our comparisons show that thermal performance at one life stage can misrepresent performance at others, and point to gains in complexity during embryogenesis, rather than subsequent gains in size or duration of exposure, as a key driver of thermal sensitivity in early life.

Constant and fluctuating temperature acclimations have similar effects on phenotypic plasticity in springtails.

Much interest exists in the extent to which constant versus fluctuating temperatures affect thermal performance traits and their phenotypic plasticity. Theory suggests that effects should vary with temperature, being especially pronounced at more extreme low (because of thermal respite) and high (because of Jensen's inequality) temperatures. Here we tested this idea by examining the effects of constant temperatures (10 to 30 °C in 5 °C increments) and fluctuating temperatures (means equal to the constant temperatures, but with fluctuations of ±5 °C) temperatures on the adult (F2) phenotypic plasticity of three thermal performance traits - critical thermal minimum (CTmin), critical thermal maximum (CTmax), and upper lethal temperature (ULT50) in ten species of springtails (Collembola) from three families (Isotomidae 7 spp.; Entomobryidae 2 spp.; Onychiuridae 1 sp.). The lowest mean CTmin value recorded here was -3.56 ± 1.0 °C for Paristoma notabilis and the highest mean CTmax was 43.1 ± 0.8 °C for Hemisotoma thermophila. The Acclimation Response Ratio for CTmin was on average 0.12 °C/°C (range: 0.04 to 0.21 °C/°C), but was much lower for CTmax (mean: 0.017 °C/°C, range: -0.015 to 0.047 °C/°C) and lower also for ULT50 (mean: 0.05 °C/°C, range: -0.007 to 0.14 °C/°C). Fluctuating versus constant temperatures typically had little effect on adult phenotypic plasticity, with effect sizes either no different from zero, or inconsistent in the direction of difference. Previous work assessing adult phenotypic plasticity of these thermal performance traits across a range of constant temperatures can thus be applied to a broader range of circumstances in springtails.

How does parental environment influence the potential for adaptation to global change?

Parental environments are regularly shown to alter the mean fitness of offspring, but their impacts on the genetic variation for fitness, which predicts adaptive capacity and is also measured on offspring, are unclear. Consequently, how parental environments mediate adaptation to environmental stressors, like those accompanying global change, is largely unknown. Here, using an ecologically important marine tubeworm in a quantitative-genetic breeding design, we tested how parental exposure to projected ocean warming alters the mean survival, and genetic variation for survival, of offspring during their most vulnerable life stage under current and projected temperatures. Offspring survival was higher when parent and offspring temperatures matched. Across offspring temperatures, parental exposure to warming altered the distribution of additive genetic variance for survival, making it covary across current and projected temperatures in a way that may aid adaptation to future warming. Parental exposure to warming also amplified nonadditive genetic variance for survival, suggesting that compatibilities between parental genomes may grow increasingly important under future warming. Our study shows that parental environments potentially have broader-ranging effects on adaptive capacity than currently appreciated, not only mitigating the negative impacts of global change but also reshaping the raw fuel for evolutionary responses to it.

Resources mediate selection on module longevity in the field.

The life histories of modular organisms are complicated, where selection and optimization can occur at both organismal and modular levels. At a modular level, growth, reproduction and death can occur in one module, independently of others. Across modular groups, there are no formal investigations of selection on module longevity. We used two field experiments to test whether selection acts on module longevity in a sessile marine invertebrate and whether selection varies across successional gradients and resource regimes. We found that selection does act on module longevity and that the strength of selection varies with environmental conditions. In environments where interspecific competition is high, selection favours colonies with longer zooid (module) longevity for colonies that initially received high levels of maternal investment. In environments where food availability is high and flow rate is low, selection also favours colonies with longer zooid longevity. These patterns of selection provide partial support for module longevity theory developed for plants. Nevertheless, that selection on module longevity is so context-dependent suggests that variation in module longevity is likely to be maintained in this system.

Should mothers provision their offspring equally? A manipulative field test.

Within-brood variation in offspring size is universal, but its causes are unclear. Theoretical explanations for within-brood variation commonly invoke bet-hedging, although alternatives consider the role of sibling competition. Despite abundant theory, empirical manipulations of within-brood variation in offspring size are rare. Using a field experiment, we investigate the consequences of unequal maternal provisioning for both maternal and offspring fitness in a marine invertebrate. We create experimental broods of siblings with identical mean, but different variance, in offspring size, and different sibling densities. Overall, more-variable broods had higher mean performance than less-variable broods, suggesting benefits of unequal provisioning that arise independently of bet-hedging. Complementarity effects drove these benefits, apparently because offspring-size variation promotes resource partitioning. We suggest that when siblings compete for the same resources, and offspring size affects niche usage, the production of more-variable broods can provide greater fitness returns given the same maternal investment; a process unanticipated by the current theory.

Field manipulations of resources mediate the transition from intraspecific competition to facilitation.

Population density affects individual performance, though its effects are often mixed. For sessile species, increases in population density typically reduce performance. Still, cases of positive density-dependence do occur in sessile systems and demand explanation. The stress gradient hypothesis (SGH) predicts that under stressful conditions, positive effects of facilitation may outweigh the negative effects of competition. While some elements of the SGH are well studied, its potential to explain intraspecific facilitation has received little attention. Further, there have been questions regarding whether the SGH holds if the stressor is a resource. Most studies of interactions between the environment and intraspecific facilitation have relied on natural environmental gradients; manipulative studies are much rarer. To test the effects of intraspecific density and resources, we manipulated resource availability over natural population densities for the marine bryozoan Watersipora subtorquata. We found negative effects of density on colony performance in low resource environments, but mainly positive density-dependence in high resource environments. By adding resources, competition effects were reduced and the positive effects of facilitation were revealed. Our results suggest that resource availability mediates the relative strength of competition and facilitation in our system. We also suggest that intraspecific facilitation is more common than may be appreciated and that environmental variation may mediate the balance between negative and positive density-dependence.

Unravelling anisogamy: egg size and ejaculate size mediate selection on morphology in free-swimming sperm.

Gamete dimorphism (anisogamy) defines the sexes in most multicellular organisms. Theoretical explanations for its maintenance usually emphasize the size-related selection pressures of sperm competition and zygote survival, assuming that fertilization of all eggs precludes selection for phenotypes that enhance fertility. In external fertilizers, however, fertilization is often incomplete due to sperm limitation, and the risk of polyspermy weakens the advantage of high sperm numbers that is predicted to limit sperm size, allowing alternative selection pressures to target free-swimming sperm. We asked whether egg size and ejaculate size mediate selection on the free-swimming sperm of Galeolaria caespitosa, a marine tubeworm with external fertilization, by comparing relationships between sperm morphology and male fertility across manipulations of egg size and sperm density. Our results suggest that selection pressures exerted by these factors may aid the maintenance of anisogamy in external fertilizers by limiting the adaptive value of larger sperm in the absence of competition. In doing so, our study offers a more complete explanation for the stability of anisogamy across the range of sperm environments typical of this mating system and identifies new potential for the sexes to coevolve via mutual selection pressures exerted by gametes at fertilization.

Why do larger mothers produce larger offspring? A test of classic theory.

Across a wide range of taxa, larger mothers produce larger offspring. Theory assumes that larger, more fecund mothers create higher local densities of siblings, and so larger mothers produce larger offspring to offset sibling competition. This assumption has been debated for over 30 yr, but direct empirical tests are surprisingly rare. Here, we test two key assumptions of classic theories that predict sibling competition drives maternal-size-offspring-size (MSOS) correlations: (1) independent effects of offspring size and sibling density on offspring performance or (2) as a product of an interaction between these two factors. To simultaneously test these alternative assumptions, we manipulate offspring size and sibling density in the marine invertebrate, Bugula neritina, and monitor offspring performance in the field. We found that, depending on the fitness metric being considered, offspring size and sibling density can either independently or interactively affect offspring performance. Yet sibling density did not affect offspring performance in the ways that classic theories assume. Given our results, it is unlikely that sibling competition drives the positive MSOS correlation observed in this species. Empirical support for these classic theories remains lacking, suggesting alternative explanations are necessary.

Revealing hidden evolutionary capacity to cope with global change.

The extent to which global change will impact the long-term persistence of species depends on their evolutionary potential to adapt to future conditions. While the number of studies that estimate the standing levels of adaptive genetic variation in populations under predicted global change scenarios is growing all the time, few studies have considered multiple environments simultaneously and even fewer have considered evolutionary potential in multivariate context. Because conditions will not be constant, adaptation to climate change is fundamentally a multivariate process so viewing genetic variances and covariances over multivariate space will always be more informative than relying on bivariate genetic correlations between traits. A multivariate approach to understanding the evolutionary capacity to cope with global change is necessary to avoid misestimating adaptive genetic variation in the dimensions in which selection will act. We assessed the evolutionary capacity of the larval stage of the marine polychaete Galeolaria caespitosa to adapt to warmer water temperatures. Galeolaria is an important habitat-forming species in Australia, and its earlier life-history stages tend to be more susceptible to stress. We used a powerful quantitative genetics design that assessed the impacts of three temperatures on subsequent survival across over 30 000 embryos across 204 unique families. We found adaptive genetic variation in the two cooler temperatures in our study, but none in the warmest temperature. Based on these results, we would have concluded that this species has very little capacity to evolve to the warmest temperature. However, when we explored genetic variation in multivariate space, we found evidence that larval survival has the potential to evolve even in the warmest temperatures via correlated responses to selection across thermal environments. Future studies should take a multivariate approach to estimating evolutionary capacity to cope with global change lest they misestimate a species' true adaptive potential.

Faster is not always better: selection on growth rate fluctuates across life history and environments.

Growth rate is increasingly recognized as a key life-history trait that may affect fitness directly rather than evolve as a by-product of selection on size or age. An ongoing challenge is to explain the abundant levels of phenotypic and genetic variation in growth rates often seen in natural populations, despite what is expected to be consistently strong selection on this trait. Such a paradox suggests limits to how contemporary growth rates evolve. We explored limits arising from variation in selection, based on selection differentials for age-specific growth rates expressed under different ecological conditions. We present results from a field experiment that measured growth rates and reproductive output in wild individuals of a colonial marine invertebrate (Hippopodina iririkiensis), replicated within and across the natural range of succession in its local community. Colony growth rates varied phenotypically throughout this range, but not all such variation was available for selection, nor was it always targeted by selection as expected. While the maintenance of both phenotypic and genetic variation in growth rate is often attributed to costs of growing rapidly, our study highlights the potential for fluctuating selection pressures throughout the life history and across environments to play an important role in this process.

Temperature and sex shape reproductive barriers in a climate change hotspot.

Climate change is altering species ranges and reproductive interactions in existing ranges, offering species new scope to mate and hybridize. The outcomes will depend on how environmental factors shape reproductive barriers across life stages, yet this is rarely assessed across the environments that species encounter in nature. We assess prezygotic and postzygotic barriers, and their dependence on temperature and parental sex, in species of a reef-building tubeworm (Galeolaria) from a fast-warming biodiversity hotspot in southern Australia. By replicating pure and reciprocal hybrid crosses across 5 temperatures spanning species' thermal ranges, we estimate thermal tolerance curves (defining niches) for crosses and reproductive isolation at each temperature. By also replicating crosses at 3 life stages, we partition the contributions of prezygotic barriers at fertilization, postzygotic barriers at embryogenesis, and postzygotic barriers at larval development to reproductive isolation. We show that barriers are weaker at fertilization and embryogenesis, but stronger and more temperature sensitive at larval development, as species diverge in thermal niche. Asymmetry of barriers between parental sexes, moreover, suggests a complex interplay between niche differentiation and maternal inheritance. Our findings point to a key role for temperature in reproductive isolation, but also challenges for predicting the fate of isolation in future climates.

Evolution of "invasion syndrome" in invasive goldenrod is not constrained by genetic trade-offs.

A suite of plant traits is thought to make weed populations highly invasive, including vigorous growth and reproduction, superior competitive ability, and high dispersal ability. Using a breeding design and a common garden experiment, we tested whether such an "invasion syndrome" has evolved in an invasive range of Solidago altissima, and whether the evolution is likely to be genetically constrained. We found an overall shift in invasive phenotypes between native North American and invasive Japanese populations. The invasive populations were taller and produced more leaves, suggesting a superior ability to exploit limited resources. The populations also produced more allelopathic compounds that can suppress competitor growth. Finally, invasive populations produced more seeds, which are smaller and are released from a greater height, indicating a potential for superior dispersal ability than the native populations. Quantitative genetics analyses found a large amount of additive genetic variation in most focal traits across native and invasive populations, with no systematic differences in its magnitude between the ranges. Genetic covariances among three traits representing invasion strategies (leaf mass, polyacetylene concentration and seed size) were small. The R metric, which measures the effect of genetic covariances on the rate of adaptation, indicated that the covariance neither constrains nor accelerates concerted evolution of these traits. The results suggest that the invasion syndrome in S. altissima has evolved in the novel range due to ample additive genetic variation, and relatively free from genetic trade-offs.

Temperature and nutrition do not interact to shape the evolution of metabolic rate.

Metabolic cold adaptation, or Krogh's rule, is the controversial hypothesis that predicts a monotonically negative relationship between metabolic rate and environmental temperature for ectotherms living along thermal clines measured at a common temperature. Macrophysiological patterns consistent with Krogh's rule are not always evident in nature, and experimentally evolved responses to temperature have failed to replicate such patterns. Hence, temperature may not be the sole driver of observed variation in metabolic rate. We tested the hypothesis that temperature, as a driver of energy demand, interacts with nutrition, a driver of energy supply, to shape the evolution of metabolic rate to produce a pattern resembling Krogh's rule. To do this, we evolved replicate lines of Drosophila melanogaster at 18, 25 or 28°C on control, low-calorie or low-protein diets. Contrary to our prediction, we observed no effect of nutrition, alone or interacting with temperature, on adult female and male metabolic rates. Moreover, support for Krogh's rule was only in females at lower temperatures. We, therefore, hypothesize that observed variation in metabolic rate along environmental clines arises from the metabolic consequences of environment-specific life-history optimization, rather than because of the direct effect of temperature on metabolic rate. This article is part of the theme issue 'The evolutionary significance of variation in metabolic rates'.

Exome-informed formulations of food proteins enhance body growth and feed conversion efficiency in ad libitum-fed mice.

Meeting requirements for dietary proteins, especially of essential amino acids (EAAs), is critical for the life-long health of living organisms. However, defining EAA targets for preparing biologically-matched nutrition that satisfies metabolic requirements for protein remains challenging. Previous research has shown the advantages of 'exome matching' in representing the specific requirement of dietary AAs, where the target dietary AA profile was derived from in silico translation of the genome of an organism, specifically responsible for protein expression (the 'exome'). However, past studies have assessed these effects in only one sex, for few parameters (body mass and composition), and have used purified diets in which protein is supplied as a mixture of individual AAs. Here, for the first time, we utilise a computational method to guide the formulation of custom protein blends and test if exome matching can be achieved at the intact protein level, through blending standard protein ingredients, ultimately leading to optimal growth, longevity and reproductive function. Mice were provided ad libitum (ad lib) access to one of the four iso-energetic protein-limited diets, two matched and two mis-matched to the mouse exome target, and fed at a fixed protein energy level of 6.2%. During or following 13-weeks of feeding, the food intake, body growth, composition and reproductive functions were measured. Compared to the two mis-matched diets, male and female animals on the exome-matched diet with protein digestibility correction applied, exhibited significantly improved growth rates and final body mass. The feed conversion efficiency in the same diet was also increased by 62% and 40% over the worst diets for males and females, respectively. Male, not female, exhibited higher accretion of lean body mass with the matched, digestibility-corrected diet. All reproductive function measures in both sexes were comparable among diets, with the exception of testicular daily sperm production in males, which was higher in the two matched diets versus the mis-matched diets. The results collectively demonstrate the pronounced advantages of exome-matching in supporting body growth and improving feed conversion efficiency in both sexes. However, the potential impact of this approach in enhancing fertility needs further investigation.

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.

Invasive ecosystem engineer selects for different phenotypes of an associated native species.

Invasive habitat-forming ecosystem engineers modify the abiotic environment and thus represent a major perturbation to many ecosystems. Because native species often persist in these invaded habitats but have no shared history with the ecosystem engineer, the engineer may impose novel selective pressure on native species. In this study, we used a phenotypic selection framework to determine whether an invasive habitat-forming ecosystem engineer (the seaweed Caulerpa taxifolia) selects for different phenotypes of a common co-occurring native species (the bivalve Anadara trapezia). Compared to unvegetated habitat, Caulerpa habitat has lower water flow, lower dissolved oxygen, and sediments are more silty and anoxic. We determined the performance consequences of variation in key functional traits that may be affected by these abiotic changes (shell morphology, gill mass, and palp mass) for Anadara transplanted into Caulerpa and unvegetated habitat. Both linear and nonlinear performance gradients in Anadara differed between habitats, and these gradients were stronger in Caulerpa compared to unvegetated sediment. Moreover, in Caulerpa alternate phenotypes performed well, and these phenotypes were different from the dominant phenotype in unvegetated sediment. By demonstrating that phenotype-performance gradients differ between habitats, we have highlighted a role for Caulerpa as an agent of selection on native species.

Thermal Performance Curves Are Shaped by Prior Thermal Environment in Early Life.

Understanding links between thermal performance and environmental variation is necessary to predict organismal responses to climate change, and remains an ongoing challenge for ectotherms with complex life cycles. Distinct life stages can differ in thermal sensitivity, experience different environmental conditions as development unfolds, and, because stages are by nature interdependent, environmental effects can carry over from one stage to affect performance at others. Thermal performance may therefore respond to carryover effects of prior thermal environments, yet detailed insights into the nature, strength, and direction of those responses are still lacking. Here, in an aquatic ectotherm whose early planktonic stages (gametes, embryos, and larvae) govern adult abundances and dynamics, we explore the effects of prior thermal environments at fertilization and embryogenesis on thermal performance curves at the end of planktonic development. We factorially manipulate temperatures at fertilization and embryogenesis, then, for each combination of prior temperatures, measure thermal performance curves for survival of planktonic development (end of the larval stage) throughout the performance range. By combining generalized linear mixed modeling with parametric bootstrapping, we formally estimate and compare curve descriptors (thermal optima, limits, and breadth) among prior environments, and reveal carryover effects of temperature at embryogenesis, but not fertilization, on thermal optima at completion of development. Specifically, thermal optima shifted to track temperature during embryogenesis, while thermal limits and breadth remained unchanged. Our results argue that key aspects of thermal performance are shaped by prior thermal environment in early life, warranting further investigation of the possible mechanisms underpinning that response, and closer consideration of thermal carryover effects when predicting organismal responses to climate change.