Anticipated effects of abiotic environmental change on intraspecific social interactions

Social interactions are ubiquitous across the animal kingdom. A variety of ecological and evolutionary processes are dependent on social interactions, such as movement, disease spread, information transmission, and density-dependent reproduction and survival. Social interactions, like any behaviour, are context dependent, varying with environmental conditions. Currently, environments are changing rapidly across multiple dimensions, becoming warmer and more variable, while habitats are increasingly fragmented and contaminated with pollutants. Social interactions are expected to change in response to these stressors and to continue to change into the future. However, a comprehensive understanding of the form and magnitude of the effects of these environmental changes on social interactions is currently lacking. Focusing on four major forms of rapid environmental change currently occurring, we review how these changing environmental gradients are expected to have immediate effects on social interactions such as communication, agonistic behaviours, and group formation, which will thereby induce changes in social organisation including mating systems, dominance hierarchies, and collective behaviour. Our review covers intraspecific variation in social interactions across environments, including studies in both the wild and in laboratory settings, and across a range of taxa. The expected responses of social behaviour to environmental change are diverse, but we identify several general themes. First, very dry, variable, fragmented, or polluted environments are likely to destabilise existing social systems. This occurs as these conditions limit the energy available for complex social interactions and affect dissimilar phenotypes differently. Second, a given environmental change can lead to opposite responses in social behaviour, and the direction of the response often hinges on the natural history of the organism in question. Third, our review highlights the fact that changes in environmental factors are not occurring in isolation: multiple factors are changing simultaneously, which may have antagonistic or synergistic effects, and more work should be done to understand these combined effects. We close by identifying methodological and analytical techniques that might help to study the response of social interactions to changing environments, highlight consistent patterns among taxa, and predict subsequent evolutionary change. We expect that the changes in social interactions that we document here will have consequences for individuals, groups, and for the ecology and evolution of populations, and therefore warrant a central place in the study of animal populations, particularly in an era of rapid environmental change.     

Habitats,stress, and evolutionary rates

Habitats of organisms are expressed as an interaction between stress intensity, magnitude of environmental fluctuations, and energy availability from resources. Under this model organisms should evolve broad biological properties defined by such physical characteristics. When energy is severely restricted under the continuing constant stress of adversity-selection, or in widely fluctuating and highly stressful environments, little evolutionary change is expected; relict species and ‘living fossils’ are the respective expectations. In rather stable abiotic environments where resources are limited habitat preferences may develop leading to specialization and ultimately adaptive radiations. On the other hand major new innovations are more likely in highly disturbed resource-rich habitats. Evidence from the living and fossil biota is presented which is consistent with these conclusions.     

Evolution of stress response in the face of unreliable environmental signals

Most organisms live in ever-changing environments, and have to cope with a range of different conditions. Often, the set of biological traits that are needed to grow, reproduce, and survive varies between conditions. As a consequence, organisms have evolved sensory systems to detect environmental signals, and to modify the expression of biological traits in response. However, there are limits to the ability of such plastic responses to cope with changing environments. Sometimes, environmental shifts might occur suddenly, and without preceding signals, so that organisms might not have time to react. Other times, signals might be unreliable, causing organisms to prepare themselves for changes that then do not occur. Here, we focus on such unreliable signals that indicate the onset of adverse conditions. We use analytical and individual-based models to investigate the evolution of simple rules that organisms use to decide whether or not to switch to a protective state. We find evolutionary transitions towards organisms that use a combination of random switching and switching in response to the signal. We also observe that, in spatially heterogeneous environments, selection on the switching strategy depends on the composition of the population, and on population size. These results are in line with recent experiments that showed that many unicellular organisms can attain different phenotypic states in a probabilistic manner, and lead to testable predictions about how this could help organisms cope with unreliable signals.     

De Novo Evolution of Complex, Global and Hierarchical Gene Regulatory Mechanisms

Gene regulatory networks exhibit complex, hierarchical features such as global regulation and network motifs. There is much debate about whether the evolutionary origins of such features are the results of adaptation, or the by-products of non-adaptive processes of DNA replication. The lack of availability of gene regulatory networks of ancestor species on evolutionary timescales makes this a particularly difficult problem to resolve. Digital organisms, however, can be used to provide a complete evolutionary record of lineages. We use a biologically realistic evolutionary model that includes gene expression, regulation, metabolism and biosynthesis, to investigate the evolution of complex function in gene regulatory networks. We discover that: (i) network architecture and complexity evolve in response to environmental complexity, (ii) global gene regulation is selected for in complex environments, (iii) complex, inter-connected, hierarchical structures evolve in stages, with energy regulation preceding stress responses, and stress responses preceding growth rate adaptations and (iv) robustness of evolved models to mutations depends on hierarchical level: energy regulation and stress responses tend not to be robust to mutations, whereas growth rate adaptations are more robust and non-lethal when mutated. These results highlight the adaptive and incremental evolution of complex biological networks, and the value and potential of studying realistic in silico evolutionary systems as a way of understanding living systems.     

Critical dynamics in the evolution of stochastic strategies for the iterated prisoner's dilemma

The observed cooperation on the level of genes, cells, tissues, and individuals has been the object of intense study by evolutionary biologists, mainly because cooperation often flourishes in biological systems in apparent contradiction to the selfish goal of survival inherent in Darwinian evolution. In order to resolve this paradox, evolutionary game theory has focused on the Prisoner's Dilemma (PD), which incorporates the essence of this conflict. Here, we encode strategies for the iterated Prisoner's Dilemma (IPD) in terms of conditional probabilities that represent the response of decision pathways given previous plays. We find that if these stochastic strategies are encoded as genes that undergo Darwinian evolution, the environmental conditions that the strategies are adapting to determine the fixed point of the evolutionary trajectory, which could be either cooperation or defection. A transition between cooperative and defective attractors occurs as a function of different parameters such as mutation rate, replacement rate, and memory, all of which affect a player's ability to predict an opponent's behavior. These results imply that in populations of players that can use previous decisions to plan future ones, cooperation depends critically on whether the players can rely on facing the same strategies that they have adapted to. Defection, on the other hand, is the optimal adaptive response in environments that change so quickly that the information gathered from previous plays cannot usefully be integrated for a response.     

Environments and evolution: interactions between stress, resource inadequacy and energetic efficiency

Evolutionary change is interpreted in terms of the near-universal ecological scenario of stressful environments. Consequently, there is a premium on the energetically efficient exploitation of resources in a resource-inadequate world. Under this environmental model, fitness can be approximated to energetic efficiency especially towards the limits of survival. Furthermore, fitness at one stage of the life-cycle should correlate with fitness at other stages, especially for development time, survival and longevity; 'good genotypes' under stress should therefore be at a premium. Conservation in the wild depends primarily on adaptation to abiotically changing habitats since towards the limits of survival, genomic variation is rarely restrictive. The balance between energetic costs under variable environments and energy from resources provides a model for interpreting evolutionary stasis, punctuational and gradual change, and specialist diversification. Ultimately, a species should be in an equilibrium between the physiology of an organism and its adaptation to the environment. The primary key to understanding evolutionary change should therefore be ecological, highlighting energy availability in a stressed world; this approach is predictive for various patterns of evolutionary change in the living and fossil biota.     

Ecological change in dynamic environments: Accounting for temporal environmental variability in studies of ocean change biology

The environmental conditions in the ocean have long been considered relatively more stable through time compared to the conditions on land. Advances in sensing technologies, however, are increasingly revealing substantial fluctuations in abiotic factors over ecologically and evolutionarily relevant timescales in the ocean, leading to a growing recognition of the dynamism of the marine environment as well as new questions about how this dynamism may influence species' vulnerability to global environmental change. In some instances, the diurnal or seasonal variability in major environmental change drivers, such as temperature, pH and seawater carbonate chemistry, and dissolved oxygen, can exceed the changes expected with continued anthropogenic global change. While ocean global change biologists have begun to experimentally test how variability in environmental conditions mediates species' responses to changes in the mean, the extensive literature on species' adaptations to temporal variability in their environment and the implications of this variability for their evolutionary responses has not been well integrated into the field. Here, we review the physiological mechanisms underlying species' responses to changes in temperature, pCO₂/pH (and other carbonate parameters), and dissolved oxygen, and discuss what is known about behavioral, plastic, and evolutionary strategies for dealing with variable environments. In addition, we discuss how exposure to variability may influence species' responses to changes in the mean conditions and highlight key research needs for ocean global change biology.     

Female polymorphism, frequency dependence, and rapid evolutionary dynamics in natural populations

Rapid evolutionary change over a few generations has been documented in natural populations. Such changes are observed as organisms invade new environments, and they are often triggered by changed interspecific interactions, such as differences in predation regimes. However, in spite of increased recognition of antagonistic male-female mating interactions, there is very limited evidence that such intraspecific interactions could cause rapid evolutionary dynamics in nature. This is because ecological and longitudinal data from natural populations have been lacking. Here we show that in a color-polymorphic damselfly species, male-female mating interactions lead to rapid evolutionary change in morph frequencies between generations. Field data and computer simulations indicate that these changes are driven by sexual conflict, in which morph fecundities are negatively affected by frequency- and density-dependent male mating harassment. These frequency-dependent processes prevent population divergence by maintaining a female polymorphism in most populations. Although these results contrast with the traditional view of how sexual conflict enhances the rate of population divergence, they are consistent with a recent theoretical model of how females may form discrete genetic clusters in response to male mating harassment.     

Communication in troubled waters: responses of fish communication systems to changing environments

Fish populations are increasingly being subjected to anthropogenic changes to their sensory environments. The impact of these changes on inter- and intra-specific communication, and its evolutionary consequences, has only recently started to receive research attention. A disruption of the sensory environment is likely to impact communication, especially with respect to reproductive interactions that help to maintain species boundaries. Aquatic ecosystems around the world are being threatened by a variety of environmental stressors, causing dramatic losses of biodiversity and bringing urgency to the need to understand how fish respond to rapid environmental changes. Here, we discuss current research on different communication systems (visual, chemical, acoustic, electric) and explore the state of our knowledge of how complex systems respond to environmental stressors using fish as a model. By far the bulk of our understanding comes from research on visual communication in the context of mate selection and competition for mates, while work on other communication systems is accumulating. In particular, it is increasingly acknowledged that environmental effects on one mode of communication may trigger compensation through other modalities. The strength and direction of selection on communication traits may vary if such compensation occurs. However, we find a dearth of studies that have taken a multimodal approach to investigating the evolutionary impact of environmental change on communication in fish. Future research should focus on the interaction between different modes of communication, especially under changing environmental conditions. Further, we see an urgent need for a better understanding of the evolutionary consequences of changes in communication systems on fish diversity.     

Rapid evolution in introduced species, 'invasive traits' and recipient communities: challenges for predicting invasive potential

The damaging effects of invasive organisms have triggered the development of Invasive Species Predictive Schemes (ISPS). These schemes evaluate biological and historical characteristics of species and prioritize those that should be the focus of exclusion, quarantine, and/or control. However, it is not clear how commonly these schemes take microevolutionary considerations into account. We review the recent literature and find that rapid evolutionary changes are common during invasions. These evolutionary changes include rapid adaptation of invaders to new environments, effects of hybridization, and evolution in recipient communities. Strikingly, we document 38 species in which the specific traits commonly associated with invasive potential (e.g. growth rate, dispersal ability, generation time) have themselves undergone evolutionary change following introduction, in some cases over very short (≤ 10 year) timescales. In contrast, our review of 29 ISPS spanning plant, animal, and microbial taxa shows that the majority (76%) envision invading species and recipient communities as static entities. Those that incorporate evolutionary considerations do so in a limited way. Evolutionary change not only affects the predictive power of these schemes, but also complicates their evaluation. We argue that including the evolutionary potential of species and communities in ISPS is overdue, present several metrics related to evolutionary potential that could be incorporated in ISPS, and provide suggestions for further research on these metrics and their performance. Finally, we argue that the fact of evolutionary change during invasions begs for added caution during risk assessment.     

Toward an integration of evolutionary biology and ecosystem science

At present, the disciplines of evolutionary biology and ecosystem science are weakly integrated. As a result, we have a poor understanding of how the ecological and evolutionary processes that create, maintain, and change biological diversity affect the flux of energy and materials in global biogeochemical cycles. The goal of this article was to review several research fields at the interfaces between ecosystem science, community ecology and evolutionary biology, and suggest new ways to integrate evolutionary biology and ecosystem science. In particular, we focus on how phenotypic evolution by natural selection can influence ecosystem functions by affecting processes at the environmental, population and community scale of ecosystem organization. We develop an eco-evolutionary model to illustrate linkages between evolutionary change (e.g. phenotypic evolution of producer), ecological interactions (e.g. consumer grazing) and ecosystem processes (e.g. nutrient cycling). We conclude by proposing experiments to test the ecosystem consequences of evolutionary changes.     

Environmental effects on the expression of life span and aging: an extreme contrast between wild and captive cohorts of Telostylinus angusticollis (Diptera: Neriidae)

Most research on life span and aging has been based on captive populations of short-lived animals; however, we know very little about the expression of these traits in wild populations of such organisms. Because life span and aging are major components of fitness, the extent to which the results of many evolutionary studies in the laboratory can be generalized to natural settings depends on the degree to which the expression of life span and aging differ in natural environments versus laboratory environments and whether such environmental effects interact with phenotypic variation. We investigated life span and aging in Telostylinus angusticollis in the wild while simultaneously estimating these parameters under a range of conditions in a laboratory stock that was recently established from the same wild population. We found that males live less than one-fifth as long and age at least twice as rapidly in the wild as do their captive counterparts. In contrast, we found no evidence of aging in wild females. These striking sex-specific differences between captive and wild flies support the emerging view that environment exerts a profound influence on the expression of life span and aging. These findings have important implications for evolutionary gerontology and, more generally, for the interpretation of fitness estimates in captive populations.     

Switching Between Cooperation and Competition in the Use of Extracellular Glucose

This paper addresses some questions related to the evolution of cooperative behaviors, in the context of energetic metabolism. Glycolysis can perform either under a dissipative working regime suitable for rapid proliferation or under an efficient regime that entails a good modus operandi under conditions of glucose shortage. A cellular mechanism allowing switching between these two regimes may represent an evolutionary achievement. Thus, we have explored the conditions that might have favored the emergence of such an accommodative mechanism. Because of an inevitable conflict for resources between individual interests and the common good, rapid and inefficient use of glucose is always favored by natural selection in spatially homogeneous environment, regardless of the external conditions. In contrast, when the space is structured, the behavior of the system is determined by its free energy content. If the fuel is abundant, the dissipative strategy dominates the space. However, under famine conditions the efficient regime represents an evolutionary stable strategy in a Harmony game. Between these two extreme situations, both metabolic regimes are engaged in a Prisoner’s Dilemma game, where the output depends on the extracellular free energy. The energy transition values that lead from one domain to another have been calculated. We conclude that an accommodative mechanism permitting alternation between dissipative and efficient regimes might have evolved in heterogeneous and highly fluctuating environments. Overall, the current work shows how evolutionary optimization and game-theoretical approaches can be complementary in providing useful insights into biochemical systems. Reviewing Editor: Dr. Antony Dean     

STRESS, EXTINCTIONS AND EVOLUTIONARY CHANGE: FROM LIVING ORGANISMS TO FOSSILS

1. Natural populations are exposed to environmental stress of varying intensities. This provides a reference point for extrapolations from the living biota to fossils and vice versa. 2. Evolutionary change is likely when there are resources in excess of maintenance and survival needs. It is largely precluded at species borders by the metabolic costs of stress; from this follows climatic tracking by species. 3. A relatively small increase in abiotic stress could underlie extinctions of stress-sensitive endemic species and the spread of stress-resistant generalist and widespread species. Widespread fossil species appear resistant to extinction under the stress level of normal background extinctions. 4. Synergistic interactions among generalized stresses should increase the likelihood of extinctions, especially for stresses with energetic consequences. 5. Some marine organisms survived the K-T mass extinction event because of stress-evasion mechanisms such as stress-resistant life-cycle stages with low metabolic rates. 6. In moderately stressed and narrowly fluctuating environments, sufficient genetic variability and metabolic energy should be available to permit adaptation. In these environments phyletic gradualism is expected. 7. In highly stressed and widely fluctuating environments, a punctuated evolutionary pattern is expected whereby stasis occurs most of the time. 8. Evolutionary patterns therefore can vary depending on the details of the interaction between stress, environmental fluctuations, energy availability and genetic variability. 9. Little evolutionary change is expected when the availability of energy is severely restricted. Examples include cave animals in stable but stressed environments and ‘living fossils’ in widely fluctuating but stressed environments. 10. Since the primary effect of abiotic stress may be at the level of energy carriers, a reductionist approach permits generalisations in considering extinctions and conditions under which diversification is likely.     

Resilience vs. historical contingency in microbial responses to environmental change

How soil processes such as carbon cycling will respond to future climate change depends on the responses of complex microbial communities, but most ecosystem models assume that microbial functional responses are resilient and can be predicted from simple parameters such as biomass and temperature. Here, we consider how historical contingencies might alter those responses because function depends on prior conditions or biota. Functional resilience can be driven by physiological, community or adaptive shifts; historical contingencies can result from the influence of historical environments or a combination of priority effects and biotic resistance. By modelling microbial population responses to environmental change, we demonstrate that historical environments can constrain soil function with the degree of constraint depending on the magnitude of change in the context of the prior environment. For example microbial assemblages from more constant environments were more sensitive to change leading to poorer functional acclimatisation compared to microbial assemblages from more fluctuating environments. Such historical contingencies can lead to deviations from expected functional responses to climate change as well as local variability in those responses. Our results form a set of interrelated hypotheses regarding soil microbial responses to climate change that warrant future empirical attention.     

Effects of the demographic transition on the genetic variances and covariances of human life‐history traits

The recent demographic transitions to lower mortality and fertility rates in most human societies have led to changes and even quick reversals in phenotypic selection pressures. This can only result in evolutionary change if the affected traits are heritable, but changes in environmental conditions may also lead to subsequent changes in the genetic variance and covariance (the G matrix) of traits. It currently remains unclear if there have been concomitant changes in the G matrix of life‐history traits following the demographic transition. Using 300 years of genealogical data from Finland, we found that four key life‐history traits were heritable both before and after the demographic transition. The estimated heritabilities allow a quantifiable genetic response to selection during both time periods, thus facilitating continued evolutionary change. Further, the G matrices remained largely stable but revealed a trend for an increased additive genetic variance and thus evolutionary potential of the population after the transition. Our results demonstrate the validity of predictions of evolutionary change in human populations even after the recent dramatic environmental change, and facilitate predictions of how our biology interacts with changing environments, with implications for global public health and demography.     

Trends and rates of microevolution in plants

Evidence for rapid evolutionary change in plants in response to changing environmental conditions is widespread in the literature. However, evolutionary change in plant populations has not been quantified using a rate metric that allows for comparisons between and within studies. One objective of this paper is to estimate rates of evolution using data from previously published studies to begin a foundation for comparison and to examine trends and rates of microevolution in plants. We use data gathered from studies of plant adaptations in response to heavy metals, herbicide, pathogens, changes in pH, global change, and novel environments. Rates of evolution are estimated in the form of two metrics, darwins and haldanes. A second objective is to demonstrate how estimated rates could be used to address specific microevolutionary questions. For example, we examine how evolutionary rate changes with time, life history correlates of evolutionary rates, and whether some types of traits evolve faster than others. We also approach the question of how rates can be used to predict patterns of evolution under novel selection pressures using two contemporary examples: introductions of non-native species to alien environments and global change.     

A Universal Definition of Life: Autonomy and Open-Ended Evolution

Life is a complex phenomenon that not only requires individual self-producing and self-sustaining systems but also a historical-collective organization of those individual systems, which brings about characteristic evolutionary dynamics. On these lines, we propose to define universally living beings as autonomous systems with open-ended evolution capacities, and we claim that all such systems must have a semi-permeable active boundary (membrane), an energy transduction apparatus (set of energy currencies) and, at least, two types of functionally interdependent macromolecular components (catalysts and records). The latter is required to articulate a 'phenotype-genotype' decoupling that leads to a scenario where the global network of autonomous systems allows for an open-ended increase in the complexity of the individual agents. Thus, the basic-individual organization of biological systems depends critically on being instructed by patterns (informational records) whose generation and reliable transmission cannot be explained but take into account the complete historical network of relationships among those systems. We conclude that a proper definition of life should consider both levels, individual and collective: living systems cannot be fully constituted without being part of the evolutionary process of a whole ecosystem. Finally, we also discuss a few practical implications of the definition for different programs of research.     

The ecological significance of time sense in animals

Time is a fundamental dimension of all biological events and it is often assumed that animals have the capacity to track the duration of experienced events (known as interval timing). Animals can potentially use temporal information as a cue during foraging, communication, predator avoidance, or navigation. Interval timing has been traditionally investigated in controlled laboratory conditions but its ecological relevance in natural environments remains unclear. While animals may time events in artificial and highly controlled conditions, they may not necessarily use temporal information in natural environments where they have access to other cues that may have more relevance than temporal information. Herein we critically evaluate the ecological contexts where interval timing has been suggested to provide adaptive value for animals. We further discuss attributes of interval timing that are rarely considered in controlled laboratory studies. Finally, we encourage consideration of ecological relevance when designing future interval-timing studies and propose future directions for such experiments.     

Environmental stress and adaptational responses: consequences for human health outcomes

With the dramatic pace of modernization of the world's population, human adaptation as a theoretical construct and paradigm will likely become a focal scientific issue involving scientists from many disciplinary areas during the 21st Century. Macro and micro environments are in rapid flux and human populations are exposed to rapid change. The concept of adaptation, at least in the field of biological anthropology and human biology, will likely remain tied to evolutionary processes and concepts of selection and fitness. In this paper, we discuss the theoretical constructs of adaptation and adaptability and select three current examples from our ongoing research that involve studies of adaptation and evolutionary processes in modernizing populations in different locations worldwide.