Mutualisms in a changing world: an evolutionary perspective

Ecology Letters (2010) 13: 1459-1474 ABSTRACT: There is growing concern that rapid environmental degradation threatens mutualistic interactions. Because mutualisms can bind species to a common fate, mutualism breakdown has the potential to expand and accelerate effects of global change on biodiversity loss and ecosystem disruption. The current focus on the ecological dynamics of mutualism under global change has skirted fundamental evolutionary issues. Here, we develop an evolutionary perspective on mutualism breakdown to complement the ecological perspective, by focusing on three processes: (1) shifts from mutualism to antagonism, (2) switches to novel partners and (3) mutualism abandonment. We then identify the evolutionary factors that may make particular classes of mutualisms especially susceptible or resistant to breakdown and discuss how communities harbouring mutualisms may be affected by these evolutionary responses. We propose a template for evolutionary research on mutualism resilience and identify conservation approaches that may help conserve targeted mutualisms in the face of environmental change.     

Local adaptation in four Iris species tested in a common-garden experiment

Local adaptation is a commonly observed result of natural selection acting in heterogeneous environment. Common-garden experiments are a method of detecting local adaptation, as well as studying phenotypic plasticity and gradients of traits. The present study aimed to analyse reaction norms of four closely-related Iris species of section Oncocyclus and to identify a role of environmentally-specific natural selection in their plastic responses. The plant vegetative and phenological, as well as performance traits were measured in a full factorial common-garden experiment with three levels of water amount and three soil types. We found a significant effect of species identity on all traits measured. Water amount and soil type affected many of the traits, but soil type did not affect the performance. There was no significant difference in the effect of water amount and soil type on performance as reflected by rhizome growth; in other words, there was no significant genotype × environment interaction for performance. Plasticity levels and directions of response were also similar among the species. We conclude that phenotypic differences among species are of genetic origin, although no adaptive value was demonstrated for them at the time and life-stages 'frame' of this experiment.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society 2009, 98 , 267–277.     

Phenology in a warming world: differences between native and non‐native plant species

Phenology is a harbinger of climate change, with many species advancing flowering in response to rising temperatures. However, there is tremendous variation among species in phenological response to warming, and any phenological differences between native and non‐native species may influence invasion outcomes under global warming. We simulated global warming in the field and found that non‐native species flowered earlier and were more phenologically plastic to temperature than natives, which did not accelerate flowering in response to warming. Non‐native species' flowering also became more synchronous with other community members under warming. Earlier flowering was associated with greater geographic spread of non‐native species, implicating phenology as a potential trait associated with the successful establishment of non‐native species across large geographic regions. Such phenological differences in both timing and plasticity between native and non‐natives are hypothesised to promote invasion success and population persistence, potentially benefiting non‐native over native species under climate change.     

Why climate change will invariably alter selection pressures on phenology

The seasonal timing of lifecycle events is closely linked to individual fitness and hence, maladaptation in phenological traits may impact population dynamics. However, few studies have analysed whether and why climate change will alter selection pressures and hence possibly induce maladaptation in phenology. To fill this gap, we here use a theoretical modelling approach. In our models, the phenologies of consumer and resource are (potentially) environmentally sensitive and depend on two different but correlated environmental variables. Fitness of the consumer depends on the phenological match with the resource. Because we explicitly model the dependence of the phenologies on environmental variables, we can test how differential (heterogeneous) versus equal (homogeneous) rates of change in the environmental variables affect selection on consumer phenology. As expected, under heterogeneous change, phenotypic plasticity is insufficient and thus selection on consumer phenology arises. However, even homogeneous change leads to directional selection on consumer phenology. This is because the consumer reaction norm has historically evolved to be flatter than the resource reaction norm, owing to time lags and imperfect cue reliability. Climate change will therefore lead to increased selection on consumer phenology across a broad range of situations.     

Resilience in reef‐building corals: The ecological and evolutionary importance of the host response to thermal stress

Coral reefs are under extreme threat due to a number of stressors, but temperature increases due to changing climate are the most severe. Rising ocean temperatures coupled with local extremes lead to extensive bleaching, where the coral‐algal symbiosis breaks down and corals may die, compromising the structure and function of reefs. Although the symbiotic nature of the coral colony has historically been a focus of research on coral resilience, the host itself is a foundational component in the response to thermal stress. Fixed effects in the coral host set trait baselines through evolutionary processes, acting on many loci of small effect to create mosaics of thermal tolerance across latitudes and individual coral reefs. These genomic differences can be strongly heritable, producing wide variation among clones of different genotypes or families of a specific larval cross. Phenotypic plasticity is overlaid on these baselines and a growing body of knowledge demonstrates the potential for acclimatization of reef‐building corals through a variety of mechanisms that promote resilience and stress tolerance. The long‐term persistence of coral reefs will require many of these mechanisms to adjust to warmer temperatures within a generation, bridging the gap to reproductive events that allow recombination of standing diversity and adaptive change. Business‐as‐usual climate scenarios will probably lead to the loss of some coral populations or species in the future, so the interaction between intragenerational effects and evolutionary pressure is critical for the survival of reefs.     

Integrating patterns of thermal tolerance and phenotypic plasticity with population genetics to improve understanding of vulnerability to warming in a widespread copepod

Differences in population vulnerability to warming are defined by spatial patterns in thermal adaptation. These patterns may be driven by natural selection over spatial environmental gradients, but can also be shaped by gene flow, especially in marine taxa with high dispersal potential. Understanding and predicting organismal responses to warming requires disentangling the opposing effects of selection and gene flow. We begin by documenting genetic divergence of thermal tolerance and developmental phenotypic plasticity. Ten populations of the widespread copepod Acartia tonsa were collected from sites across a large thermal gradient, ranging from the Florida Keys to Northern New Brunswick, Canada (spanning over 20° latitude). Thermal performance curves (TPCs) from common garden experiments revealed local adaptation at the sampling range extremes, with thermal tolerance increasing at low latitudes and decreasing at high latitudes. The opposite pattern was observed in phenotypic plasticity, which was strongest at high latitudes. No relationship was observed between phenotypic plasticity and environmental variables. Instead, the results are consistent with the hypothesis of a trade‐off between thermal tolerance and the strength of phenotypic plasticity. Over a large portion of the sampled range, however, we observed a remarkable lack of differentiation of TPCs. To examine whether this lack of divergence is the result of selection for a generalist performance curve or constraint by gene flow, we analyzed cytochrome oxidase I mtDNA sequences, which revealed four distinct genetic clades, abundant genetic diversity, and widely distributed haplotypes. Strong divergence in thermal performance within genetic clades, however, suggests that the pace of thermal adaptation can be relatively rapid. The combined insight from the laboratory physiological experiments and genetic data indicate that gene flow constrains differentiation of TPCs. This balance between gene flow and selection has implications for patterns of vulnerability to warming. Taking both genetic differentiation and phenotypic plasticity into account, our results suggest that local adaptation does not increase vulnerability to warming, and that low‐latitude populations in general may be more vulnerable to predicted temperature change over the next century.     

Non-climatic thermal adaptation: implications for species' responses to climate warming

There is considerable interest in understanding how ectothermic animals may physiologically and behaviourally buffer the effects of climate warming. Much less consideration is being given to how organisms might adapt to non-climatic heat sources in ways that could confound predictions for responses of species and communities to climate warming. Although adaptation to non-climatic heat sources (solar and geothermal) seems likely in some marine species, climate warming predictions for marine ectotherms are largely based on adaptation to climatically relevant heat sources (air or surface sea water temperature). Here, we show that non-climatic solar heating underlies thermal resistance adaptation in a rocky–eulittoral-fringe snail. Comparisons of the maximum temperatures of the air, the snail''s body and the rock substratum with solar irradiance and physiological performance show that the highest body temperature is primarily controlled by solar heating and re-radiation, and that the snail''s upper lethal temperature exceeds the highest climatically relevant regional air temperature by approximately 22°C. Non-climatic thermal adaptation probably features widely among marine and terrestrial ectotherms and because it could enable species to tolerate climatic rises in air temperature, it deserves more consideration in general and for inclusion into climate warming models.     

A warmer environment can reduce sociability in an ectotherm

The costs and benefits of being social vary with environmental conditions, so individuals must weigh the balance between these trade-offs in response to changes in the environment. Temperature is a salient environmental factor that may play a key role in altering the costs and benefits of sociality through its effects on food availability, predator abundance, and other ecological parameters. In ectotherms, changes in temperature also have direct effects on physiological traits linked to social behaviour, such as metabolic rate and locomotor performance. In light of climate change, it is therefore important to understand the potential effects of temperature on sociality. Here, we took the advantage of a ‘natural experiment’ of threespine sticklebacks from contrasting thermal environments in Iceland: geothermally warmed water bodies (warm habitats) and adjacent ambient-temperature water bodies (cold habitats) that were either linked (sympatric) or physically distinct (allopatric). We first measured the sociability of wild-caught adult fish from warm and cold habitats after acclimation to a low and a high temperature. At both acclimation temperatures, fish from the allopatric warm habitat were less social than those from the allopatric cold habitat, whereas fish from sympatric warm and cold habitats showed no differences in sociability. To determine whether differences in sociability between thermal habitats in the allopatric population were heritable, we used a common garden breeding design where individuals from the warm and the cold habitat were reared at a low or high temperature for two generations. We found that sociability was indeed heritable but also influenced by rearing temperature, suggesting that thermal conditions during early life can play an important role in influencing social behaviour in adulthood. By providing the first evidence for a causal effect of rearing temperature on social behaviour, our study provides novel insights into how a warming world may influence sociality in animal populations.     

Integrating metabolic performance,thermal tolerance,and plasticity enables for more accurate predictions on species vulnerability to acute and chronic effects of global warming

Predicting species vulnerability to global warming requires a comprehensive, mechanistic understanding of sublethal and lethal thermal tolerances. To date, however, most studies investigating species physiological responses to increasing temperature have focused on the underlying physiological traits of either acute or chronic tolerance in isolation. Here we propose an integrative, synthetic approach including the investigation of multiple physiological traits (metabolic performance and thermal tolerance), and their plasticity, to provide more accurate and balanced predictions on species and assemblage vulnerability to both acute and chronic effects of global warming. We applied this approach to more accurately elucidate relative species vulnerability to warming within an assemblage of six caridean prawns occurring in the same geographic, hence macroclimatic, region, but living in different thermal habitats. Prawns were exposed to four incubation temperatures (10, 15, 20 and 25 °C) for 7 days, their metabolic rates and upper thermal limits were measured, and plasticity was calculated according to the concept of Reaction Norms, as well as Q₁₀ for metabolism. Compared to species occupying narrower/more stable thermal niches, species inhabiting broader/more variable thermal environments (including the invasive Palaemon macrodactylus) are likely to be less vulnerable to extreme acute thermal events as a result of their higher upper thermal limits. Nevertheless, they may be at greater risk from chronic exposure to warming due to the greater metabolic costs they incur. Indeed, a trade‐off between acute and chronic tolerance was apparent in the assemblage investigated. However, the invasive species P. macrodactylus represents an exception to this pattern, showing elevated thermal limits and plasticity of these limits, as well as a high metabolic control. In general, integrating multiple proxies for species physiological acute and chronic responses to increasing temperature helps providing more accurate predictions on species vulnerability to warming.     

Racing against change: understanding dispersal and persistence to improve species' conservation prospects

Climate change is contributing to the widespread redistribution, and increasingly the loss, of species. Geographical range shifts among many species were detected rapidly after predictions of the potential importance of climate change were specified 35 years ago: species are shifting their ranges towards the poles and often to higher elevations in mountainous areas. Early tests of these predictions were largely qualitative, though extraordinarily rapid and broadly based, and statistical tests distinguishing between climate change and other global change drivers provided quantitative evidence that climate change had already begun to cause species’ geographical ranges to shift. I review two mechanisms enabling this process, namely development of approaches for accounting for dispersal that contributes to range expansion, and identification of factors that alter persistence and lead to range loss. Dispersal in the context of range expansion depends on an array of processes, like population growth rates in novel environments, rates of individual species movements to new locations, and how quickly areas of climatically tolerable habitat shift. These factors can be tied together in well-understood mathematical frameworks or modelled statistically, leading to better prediction of extinction risk as climate changes. Yet, species'' increasing exposures to novel climate conditions can exceed their tolerances and raise the likelihood of local extinction and consequent range losses. Such losses are the consequence of processes acting on individuals, driven by factors, such as the growing frequency and severity of extreme weather, that contribute local extinction risks for populations and species. Many mechanisms can govern how species respond to climate change, and rapid progress in global change research creates many opportunities to inform policy and improve conservation outcomes in the early stages of the sixth mass extinction.     

Rethinking species' ability to cope with rapid climate change

Ongoing climate change is assumed to be exceptional because of its unprecedented velocity. However, new geophysical research suggests that dramatic climatic changes during the Late Pleistocene occurred extremely rapid, over just a few years. These abrupt climatic changes may have been even faster than contemporary ones, but relatively few continent‐wide extinctions of species have been documented for these periods. This raises questions about the ability of extant species to adapt to ongoing climate change. We propose that the advances in geophysical research challenge current views about species' ability to cope with climate change, and that lessons must be learned for modelling future impacts of climate change on species.     

Keeping up with a warming world; assessing the rate of adaptation to climate change

The pivotal question in the debate on the ecological effects of climate change is whether species will be able to adapt fast enough to keep up with their changing environment. If we establish the maximal rate of adaptation, this will set an upper limit to the rate at which temperatures can increase without loss of biodiversity.The rate of adaptation will primarily be set by the rate of microevolution since (i) phenotypic plasticity alone is not sufficient as reaction norms will no longer be adaptive and hence microevolution on the reaction norm is needed, (ii) learning will be favourable to the individual but cannot be passed on to the next generations, (iii) maternal effects may play a role but, as with other forms of phenotypic plasticity, the response of offspring to the maternal cues will no longer be adaptive in a changing environment, and (iv) adaptation via immigration of individuals with genotypes adapted to warmer environments also involves microevolution as these genotypes are better adapted in terms of temperature, but not in terms of, for instance, photoperiod.Long-term studies on wild populations with individually known animals play an essential role in detecting and understanding the temporal trends in life-history traits, and to estimate the heritability of, and selection pressures on, life-history traits. However, additional measurements on other trophic levels and on the mechanisms underlying phenotypic plasticity are needed to predict the rate of microevolution, especially under changing conditions.Using this knowledge on heritability of, and selection on, life-history traits, in combination with climate scenarios, we will be able to predict the rate of adaptation for different climate scenarios. The final step is to use ecoevolutionary dynamical models to make the link to population viability and from there to biodiversity loss for those scenarios where the rate of adaptation is insufficient.     

Temperature‐size responses alter food chain persistence across environmental gradients

Body‐size reduction is a ubiquitous response to global warming alongside changes in species phenology and distributions. However, ecological consequences of temperature‐size (TS) responses for community persistence under environmental change remain largely unexplored. Here, we investigated the interactive effects of warming, enrichment, community size structure and TS responses on a three‐species food chain using a temperature‐dependent model with empirical parameterisation. We found that TS responses often increase community persistence, mainly by modifying consumer‐resource size ratios and thereby altering interaction strengths and energetic efficiencies. However, the sign and magnitude of these effects vary with warming and enrichment levels, TS responses of constituent species, and community size structure. We predict that the consequences of TS responses are stronger in aquatic than in terrestrial ecosystems, especially when species show different TS responses. We conclude that considering the links between phenotypic plasticity, environmental drivers and species interactions is crucial to better predict global change impacts on ecosystem diversity and stability.     

Towards a mechanistic understanding of dispersal evolution in plants: conservation implications

Aim A species’ dispersal characteristics will play a key role in determining its likely fate during a period of environmental change. However, these characteristics are not constant within a species – instead, there is often both considerable interpopulation and interindividual variability. Also changes in selection pressures can result in the evolution of dispersal characteristics, with knock‐on consequences for a species’ population dynamics. Our aim here is to make our theoretical understanding of dispersal evolution more conservation‐relevant by moving beyond the rather abstract, phenomenological models that have dominated the literature towards a more mechanism‐based approach. Methods We introduce a continuous‐space, individual‐based model for wind‐dispersed plants where release height is determined by an individual’s ‘genotype’. A mechanistic wind dispersal model is used to simulate seed dispersal. Selection acts on variation in release height that is generated through mutation. Results We confirm that, when habitat is fragmented, both evolutionary rescue and evolutionary suicide remain possible outcomes when a mechanistic dispersal model is used. We also demonstrate the potential for what we term evolutionary entrapment. A population that under some conditions can evolve to be sufficiently dispersive that it expands rapidly across a fragmented landscape can, under different conditions, become trapped by a combination of limited dispersal and a large gap between patches. Conclusions While developing evolutionary models to be used as conservation tools is undoubtedly a challenge, we believe that, with a concerted collaborative effort linking the knowledge and methods of ecologists, evolutionary biologists and geneticists, it is an achievable aim.     

Different ways to die in a changing world: Consequences of climate change for tree species performance and survival through an ecophysiological perspective

Anthropogenic activities such as uncontrolled deforestation and increasing greenhouse gas emissions are responsible for triggering a series of environmental imbalances that affect the Earth's complex climate dynamics. As a consequence of these changes, several climate models forecast an intensification of extreme weather events over the upcoming decades, including heat waves and increasingly severe drought and flood episodes. The occurrence of such extreme weather will prompt profound changes in several plant communities, resulting in massive forest dieback events that can trigger a massive loss of biodiversity in several biomes worldwide. Despite the gravity of the situation, our knowledge regarding how extreme weather events can undermine the performance, survival, and distribution of forest species remains very fragmented. Therefore, the present review aimed to provide a broad and integrated perspective of the main biochemical, physiological, and morpho‐anatomical disorders that may compromise the performance and survival of forest species exposed to climate change factors, particularly drought, flooding, and global warming. In addition, we also discuss the controversial effects of high CO₂ concentrations in enhancing plant growth and reducing the deleterious effects of some extreme climatic events. We conclude with a discussion about the possible effects that the factors associated with the climate change might have on species distribution and forest composition.     

Genetic variation and plasticity of thorax length and wing length in Drosophila aldrichi and D. buzzatii

Reaction norms across three temperatures of development were measured for thorax length, wing length and wing length/thorax length ratio for ten isofemale lines from each of two populations of Drosophila aldrichi and D. buzzatii. Means for thorax and wing length in both species were larger at 24 °C than at either 18 °C or 31 °C, with the reduction in size at 18 °C most likely due to a nutritional constraint. Although females were larger than males, the sexes were not different for wing length/thorax length ratio. The plasticity of the traits differed between species and between populations of each species, with genetic variation in plasticity similar for the two species from one locality, but much higher for D. aldrichi from the other. Estimates of heritabilities for D. aldrichi generally were higher at 18 °C and 24 °C than at 31 °C, but for D. buzzatii they were highest at 31 °C, although heritabilities were not significantly different between species at any temperature. Additive genetic variances for D. aldrichi showed trends similar to that for heritability, being highest at 18 °C and decreasing as temperature increased. For D. buzzatii, however, additive genetic variances were lowest at 24 °C. These results are suggestive that genetic variation for body size characters is increased in more stressful environments. Thorax and wing lengths showed significant genetic correlations that were not different between the species, but the genetic correlations between each of these traits and their ratio were significantly different. For D. aldrichi, genetic variation in the wing length/thorax length ratio was due primarily to variation in thorax length, while for D. buzzatii, it was due primarily to variation in wing length. The wing length/thorax length ratio, which is the inverse of wing loading, decreased linearly as temperature increased, and it is suggested that this ratio may be of greater adaptive significance than either of its components.