Cameron K. Ghalambor

Impacts of climate warming on terrestrial ectotherms across latitude

The impact of anthropogenic climate change on terrestrial organisms is often predicted to increase with latitude, in parallel with the rate of warming. Yet the biological impact of rising temperatures also depends on the physiological sensitivity of organisms to temperature change. We integrate empirical fitness curves describing the thermal tolerance of terrestrial insects from around the world with the projected geographic distribution of climate change for the next century to estimate the direct impact of warming on insect fitness across latitude. The results show that warming in the tropics, although relatively small in magnitude, is likely to have the most deleterious consequences because tropical insects are relatively sensitive to temperature change and are currently living very close to their optimal temperature. In contrast, species at higher latitudes have broader thermal tolerance and are living in climates that are currently cooler than their physiological optima, so that warming may even enhance their fitness. Available thermal tolerance data for several vertebrate taxa exhibit similar patterns, suggesting that these results are general for terrestrial ectotherms. Our analyses imply that, in the absence of ameliorating factors such as migration and adaptation, the greatest extinction risks from global warming may be in the tropics, where biological diversity is also greatest.

Effect of extrinsic mortality on the evolution of senescence in guppies.

Classical theories for the evolution of senescence predict that organisms that experience low mortality rates attributable to external factors, such as disease or predation, will evolve a later onset of senescence. Here we use patterns of senescence in guppies derived from natural populations that differ in mortality risk to evaluate the generality of these predictions. We have previously found that populations experiencing higher mortality rates evolve earlier maturity and invest more in reproduction, as predicted by evolutionary theory. We report here that these same populations do not have an earlier onset of senescence with respect to either mortality or reproduction but do with respect to swimming performance, which assesses neuromuscular function. This mosaic pattern of senescence challenges the generality of the association between decreased extrinsic mortality and delayed senescence and invites consideration of more derived theories for the evolution of senescence.

Constraints on Adaptive Evolution: The functional trade-off between reproduction and fast-start swimming performance in the Trinidadian guppy (Poecilia reticulata)

The empirical study of natural selection reveals that adaptations often involve trade‐offs between competing functions. Because natural selection acts on whole organisms rather than isolated traits, adaptive evolution may be constrained by the interaction between traits that are functionally integrated. Yet, few attempts have been made to characterize how and when such constraints are manifested or whether they limit the adaptive divergence of populations. Here we examine the consequences of adaptive life‐history evolution on locomotor performance in the live‐bearing guppy. In response to increased predation from piscivorous fish, Trinidadian guppies evolve an increased allocation of resources toward reproduction. These populations are also under strong selection for rapid fast‐start swimming performance to evade predators. Because embryo development increases a female’s wet mass as she approaches parturition, an increased investment in reproductive allocation should impede fast‐start performance. We find evidence for adaptive but constrained evolution of fast‐start swimming performance in laboratory trials conducted on second‐generation lab‐reared fish. Female guppies from high‐predation localities attain a faster acceleration and velocity and travel a greater distance during fast‐start swimming trials. However, velocity and distance traveled decline more rapidly over the course of pregnancy in these same females, thus reducing the magnitude of divergence in swimming performance between high‐ and low‐predation populations. This functional trade‐off between reproduction and swimming performance reveals how different aspects of the phenotype are integrated and highlights the complexity of adaptation at the whole‐organism level.

Macrophysiology: A Conceptual Reunification

Widespread recognition of the importance of biological studies at large spatial and temporal scales, particularly in the face of many of the most pressing issues facing humanity, has fueled the argument that there is a need to reinvigorate such studies in physiological ecology through the establishment of a macrophysiology. Following a period when the fields of ecology and physiological ecology had been regarded as largely synonymous, studies of this kind were relatively commonplace in the first half of the twentieth century. However, such large‐scale work subsequently became rather scarce as physiological studies concentrated on the biochemical and molecular mechanisms underlying the capacities and tolerances of species. In some sense, macrophysiology is thus an attempt at a conceptual reunification. In this article, we provide a conceptual framework for the continued development of macrophysiology. We subdivide this framework into three major components: the establishment of macrophysiological patterns, determining the form of those patterns (the very general ways in which they are shaped), and understanding the mechanisms that give rise to them. We suggest ways in which each of these components could be developed usefully.

Non-adaptive plasticity potentiates rapid adaptive evolution of gene expression in nature.

Phenotypic plasticity is the capacity for an individual genotype to produce different phenotypes in response to environmental variation. Most traits are plastic, but the degree to which plasticity is adaptive or non-adaptive depends on whether environmentally induced phenotypes are closer or further away from the local optimum. Existing theories make conflicting predictions about whether plasticity constrains or facilitates adaptive evolution. Debate persists because few empirical studies have tested the relationship between initial plasticity and subsequent adaptive evolution in natural populations. Here we show that the direction of plasticity in gene expression is generally opposite to the direction of adaptive evolution. We experimentally transplanted Trinidadian guppies (Poecilia reticulata) adapted to living with cichlid predators to cichlid-free streams, and tested for evolutionary divergence in brain gene expression patterns after three to four generations. We find 135 transcripts that evolved parallel changes in expression within the replicated introduction populations. These changes are in the same direction exhibited in a native cichlid-free population, suggesting rapid adaptive evolution. We find 89% of these transcripts exhibited non-adaptive plastic changes in expression when the source population was reared in the absence of predators, as they are in the opposite direction to the evolved changes. By contrast, the remaining transcripts exhibiting adaptive plasticity show reduced population divergence. Furthermore, the most plastic transcripts in the source population evolved reduced plasticity in the introduction populations, suggesting strong selection against non-adaptive plasticity. These results support models predicting that adaptive plasticity constrains evolution, whereas non-adaptive plasticity potentiates evolution by increasing the strength of directional selection. The role of non-adaptive plasticity in evolution has received relatively little attention; however, our results suggest that it may be an important mechanism that predicts evolutionary responses to new environments.Phenotypic plasticity is the capacity for an individual genotype to produce different phenotypes in response to environmental variation. Most traits are plastic, but the degree to which plasticity is adaptive or non-adaptive depends on whether environmentally induced phenotypes are closer or further away from the local optimum. Existing theories make conflicting predictions about whether plasticity constrains or facilitates adaptive evolution. Debate persists because few empirical studies have tested the relationship between initial plasticity and subsequent adaptive evolution in natural populations. Here we show that the direction of plasticity in gene expression is generally opposite to the direction of adaptive evolution. We experimentally transplanted Trinidadian guppies (Poecilia reticulata) adapted to living with cichlid predators to cichlid-free streams, and tested for evolutionary divergence in brain gene expression patterns after three to four generations. We find 135 transcripts that evolved parallel changes in expression within the replicated introduction populations. These changes are in the same direction exhibited in a native cichlid-free population, suggesting rapid adaptive evolution. We find 89% of these transcripts exhibited non-adaptive plastic changes in expression when the source population was reared in the absence of predators, as they are in the opposite direction to the evolved changes. By contrast, the remaining transcripts exhibiting adaptive plasticity show reduced population divergence. Furthermore, the most plastic transcripts in the source population evolved reduced plasticity in the introduction populations, suggesting strong selection against non-adaptive plasticity. These results support models predicting that adaptive plasticity constrains evolution, whereas non-adaptive plasticity potentiates evolution by increasing the strength of directional selection. The role of non-adaptive plasticity in evolution has received relatively little attention; however, our results suggest that it may be an important mechanism that predicts evolutionary responses to new environments.

EVOLUTION OF LIFE HISTORIES ALONG ELEVATIONAL GRADIENTS: TRADE‐OFF BETWEEN PARENTAL CARE AND FECUNDITY

Life history responses to environmental conditions include a combination of fecundity-survival schedules and behavioral strategies that yield the highest fitness in a given environment. In this study, we examined the pattern of covariation in avian life history strategies along an elevational gradient by comparing variation in life history traits, including most components of parental care, between phylogenetically paired taxa from low- and high-elevation sites. We found that high-elevation species had significantly lower annual fecundity but provided greater parental care to their offspring. However, a strong negative relationship between offspring number and duration of parental care along the elevational gradient suggested that high-elevation species were shifting investment from offspring number toward offspring quality. Although adult survival did not differ between high- and low-elevation species, higher juvenile survival may have compensated for lower annual fecundity in high-elevation species. The elevation at which breeding occurred strong- ly influenced the partitioning of parental behavior between sexes. Male participation in nestling provisioning was significantly greater in high-elevation species. In turn, altitudinal variation in the frequency of biparental care closely covaries with the intensity of sexual selection, ultimately resulting in the strong elevational pattern of sexual dimorphism. More- over, elevational variation in costs of development and maintenance of secondary sexual traits constitutes an additional effect on fecundity-survival schedules along elevational gradients. Thus, a trade-off between fecundity and parental care, and associated interactions among morphological, life history, and behavioral traits play important roles in the evolution of life history strategies in birds.

Multi-trait Selection, Adaptation, and Constraints on the Evolution of Burst Swimming Performance

Abstract Whole organism performance represents the integration of numerous physiological, morphological, and behavioral traits. How adaptive changes in performance evolve therefore requires an understanding of how selection acts on multiple integrated traits. Two approaches that lend themselves to studying the evolution of performance in natural populations are the use of quantitative genetics models for estimating the strength of selection acting on multiple quantitative traits and ecological genetic comparisons of populations exhibiting phenotypic differences correlated with environmental variation. In both cases, the ultimate goal is to understand how suites of traits and trade-offs between competing functions respond to natural selection. Here we consider how these two complimentary approaches can be applied to study the adaptive evolution of escape performance in fish. We first present an extension of Arnolds (1983) quantitative genetic approach that explicitly considers how trade-offs between different components of performance interact with the underlying genetics. We propose that such a model can reveal the conditions under which multiple selection pressures will cause adaptive change in traits that influence more than one component of fitness. We then review work on the Atlantic silversides and Trinidadian guppies as two case studies where an ecological genetics approach has been successfully applied to evaluate how the evolution of escape performance trades-off with other components of fitness. We conclude with the general lesson that whole organism performance is embedded in a complex phenotype, and that the net outcome of selection acting on different aspects of the organism will often result in a compromise among competing influences.

Parental investment strategies in two species of nuthatch vary with stage-specific predation risk and reproductive effort.

Life-history theory predicts that differences in reproductive effort and residual reproductive value among species should result in differences in the level of risk that parents are willing to tolerate to themselves versus their offspring. Specifically, highly fecund and shorter-lived species are expected to place greater value in current offspring than themselves, whereas less fecund and longer-lived species are expected to place greater value in their own survival and future breeding opportunities. Here, we test the prediction that parental investment decisions are correlated with life histories by comparing risk-taking behaviour in two species of nuthatch that differ in reproductive effort: the white-breasted nuthatch, Sitta carolinensis (more fecund, lower survival) and the red-breasted nuthatch, S. canadensis (less fecund, higher survival). We experimentally manipulated stage-specific predation risk by presenting models of an adult predator (hawk) and an egg predator (wren) and measured the willingness of males to feed incubating females on the nest. We found that both species of nuthatch responded to predators by increasing the length of time between visits and aborting more visits to the nest. However, as predicted by their life histories, S. carolinensis displayed a significantly stronger response to the egg predator, whereas S. canadensis responded more strongly to the adult predator. Thus, species can differ in their willingness to tolerate risk to themselves and their young, and such differences appear to be related to differences in investment in current reproduction and the probability of future survival. Copyright 2000 The Association for the Study of Animal Behaviour.

Males Feeding Females During Incubation. I. Required by Microclimate or Constrained by Nest Predation

Nest attentiveness (percentage of time spent on the nest) during incubation represents a parent‐offspring conflict; incubating birds must balance a trade‐off between caring for embryos by staying on the nest versus caring for themselves by getting off the nest to forage. For species in which females are the sole incubator, males can potentially affect this trade‐off and increase nest attentiveness by feeding incubating females on the nest (incubation feeding). Increased nest attentiveness may be required when local microclimate conditions are harsh and thereby require greater incubation feeding (microclimate hypothesis). Alternatively, incubation feeding may be constrained by risk of attracting nest predators (nest predation hypothesis), which in turn may constrain female nest attentiveness because of energy limitation. We show that incubation feeding rates are much greater among cavity‐nesting than among coexisting open‐nesting birds. Under the microclimate hypothesis, the greater incubation feeding rates of cavity‐nesting birds generate the prediction that microclimate should be harsher than for open‐nesting birds. Our results reject this hypothesis because we found the opposite pattern; cavity‐nesting birds experienced more moderate (less variable) microclimates that were less often below temperatures (i.e., 16°C) that can negatively impact eggs compared with open‐nesting species. In contrast, incubation feeding rates were highly negatively correlated with nest predation both within and between the two nest types, supporting the nest predation hypothesis. Incubation feeding in turn was positively correlated with nest attentiveness. Thus, nest predation may indirectly affect female incubation behavior by directly affecting incubation feeding by the male.

Constraints on the evolution of phenotypic plasticity: limits and costs of phenotype and plasticity

Phenotypic plasticity is ubiquitous and generally regarded as a key mechanism for enabling organisms to survive in the face of environmental change. Because no organism is infinitely or ideally plastic, theory suggests that there must be limits (for example, the lack of ability to produce an optimal trait) to the evolution of phenotypic plasticity, or that plasticity may have inherent significant costs. Yet numerous experimental studies have not detected widespread costs. Explicitly differentiating plasticity costs from phenotype costs, we re-evaluate fundamental questions of the limits to the evolution of plasticity and of generalists vs specialists. We advocate for the view that relaxed selection and variable selection intensities are likely more important constraints to the evolution of plasticity than the costs of plasticity. Some forms of plasticity, such as learning, may be inherently costly. In addition, we examine opportunities to offset costs of phenotypes through ontogeny, amelioration of phenotypic costs across environments, and the condition-dependent hypothesis. We propose avenues of further inquiry in the limits of plasticity using new and classic methods of ecological parameterization, phylogenetics and omics in the context of answering questions on the constraints of plasticity. Given plasticity’s key role in coping with environmental change, approaches spanning the spectrum from applied to basic will greatly enrich our understanding of the evolution of plasticity and resolve our understanding of limits.