Climate velocities and species tracking in global mountain regions.

Mountain ranges contain high concentrations of endemic species and are indispensable refugia for lowland species that are facing anthropogenic climate change1,2. Forecasting biodiversity redistribution hinges on assessing whether species can track shifting isotherms as the climate warms3,4. However, a global analysis of the velocities of isotherm shifts along elevation gradients is hindered by the scarcity of weather stations in mountainous regions5. Here we address this issue by mapping the lapse rate of temperature (LRT) across mountain regions globally, both by using satellite data (SLRT) and by using the laws of thermodynamics to account for water vapour6 (that is, the moist adiabatic lapse rate (MALRT)). By dividing the rate of surface warming from 1971 to 2020 by either the SLRT or the MALRT, we provide maps of vertical isotherm shift velocities. We identify 17 mountain regions with exceptionally high vertical isotherm shift velocities (greater than 11.67 m per year for the SLRT; greater than 8.25 m per year for the MALRT), predominantly in dry areas but also in wet regions with shallow lapse rates; for example, northern Sumatra, the Brazilian highlands and southern Africa. By linking these velocities to the velocities of species range shifts, we report instances of close tracking in mountains with lower climate velocities. However, many species lag behind, suggesting that range shift dynamics would persist even if we managed to curb climate-change trajectories. Our findings are key for devising global conservation strategies, particularly in the 17 high-velocity mountain regions that we have identified.

Environmental quality mediates the ecological dominance of cooperatively breeding birds.

Although social species as diverse as humans and ants are among the most abundant organisms on Earth, animals cooperate and form groups for many reasons. How these different reasons for grouping affect a species' ecological dominance remains unknown. Here we use a theoretical model to demonstrate that the different fitness benefits that animals receive by forming groups depend on the quality of their environment, which in turn impacts their ecological dominance and resilience to global change. We then test the model's key predictions using phylogenetic comparative analysis of >6500 bird species. As predicted, we find that cooperative breeders occurring in harsh and fluctuating environments have larger ranges and greater abundances than non-cooperative breeders, but cooperative breeders occurring in benign and stable environments do not. Using our model, we further show that social species living in harsh and fluctuating environments will be less vulnerable to climate change than non-social species.

Higher temperature variability in deforested mountain regions impacts the competitive advantage of nocturnal species.

Deforestation is a major contributor to biodiversity loss, yet the impact of forest loss on daily microclimate variability and its implications for species with different daily activity patterns remain poorly understood. Using a recently developed microclimate model, we investigated the effects of deforestation on the daily temperature range (DTR) in low-elevation tropical regions and high-elevation temperate regions. Our results show that deforestation substantially increases DTR in these areas, suggesting a potential impact on species interactions. To test this hypothesis, we studied the competitive interactions between nocturnal burying beetles and all-day-active blowfly maggots in forested and deforested habitats in Taiwan. We show that deforestation leads to increased DTR at higher elevations, which enhances the competitiveness of blowfly maggots during the day and leads to a higher failure rate of carcass burial by the beetles at night. Thus, deforestation-induced temperature variability not only modulates exploitative competition between species with different daily activity patterns, but also likely exacerbates the negative impacts of climate change on nocturnal organisms. In order to limit potential adverse effects on species interactions and their ecological functions, our study highlights the need to protect forests, especially in areas where deforestation can greatly alter temperature variability.

Cooperation and Lateral Forces: Moving Beyond Bottom-Up and Top-Down Drivers of Animal Population Dynamics.

Biologists have long known that animal population dynamics are regulated by a combination of bottom-up (resource availability) and top-down forces (predation). Yet, economists have argued that human population dynamics can also be influenced by intraspecific cooperation. Despite awareness of the role of interspecific cooperation (mutualism) in influencing resource availability and animal population dynamics, the role of intraspecific cooperation (sociality) under different environmental conditions has rarely been considered. Here we examine the role of what we call "lateral forces" that act within populations and interact with external top-down and bottom-up forces in influencing population dynamics using an individual-based model linking environmental quality, intraspecific cooperation, and population size. We find that the proportion of cooperators is higher when the environment is poor and population sizes are greatest under intermediate resources levels due to the contrasting effects of resource availability on behavior and population size. We also show that social populations are more resilient to environmental change than non-social ones because the benefits of intraspecific cooperation can outweigh the effects of constrained resource availability. Our study elucidates the complex relationship between environmental harshness, cooperation, and population dynamics, which is important for understanding the ecological consequences of cooperation.

Antagonistic effects of long- and short-term environmental variation on species coexistence.

Assessing the impact of environmental fluctuations on species coexistence is critical for understanding biodiversity loss and the ecological impacts of climate change. Yet determining how properties like the intensity, frequency or duration of environmental fluctuations influence species coexistence remains challenging, presumably because previous studies have focused on indefinite coexistence. Here, we model the impact of environmental fluctuations at different temporal scales on species coexistence over a finite time period by employing the concepts of time-windowed averaging and performance curves to incorporate temporal niche differences within a stochastic Lotka-Volterra model. We discover that short- and long-term environmental variability has contrasting effects on transient species coexistence, such that short-term variation favours species coexistence, whereas long-term variation promotes competitive exclusion. This dichotomy occurs because small samples (e.g. environmental changes over long time periods) are more likely to show large deviations from the expected mean and are more difficult to predict than large samples (e.g. environmental changes over short time periods), as described in the central limit theorem. Consequently, we show that the complex set of relationships among environmental fluctuations and species coexistence found in previous studies can all be synthesized within a general framework by explicitly considering both long- and short-term environmental variation.

Social rank modulates how environmental quality influences cooperation and conflict within animal societies.

Although dominance hierarchies occur in most societies, our understanding of how these power structures influence individual investment in cooperative and competitive behaviours remains elusive. Both conflict and cooperation in animal societies are often environmentally regulated, yet how individuals alter their cooperative and competitive investments as environmental quality changes remain unclear. Using game theoretic modelling, we predict that individuals of all ranks will invest more in cooperation and less in social conflict in harsh environments than individuals of the same ranks in benign environments. Counterintuitively, low-ranking subordinates should increase their investment in cooperation proportionally more than high-ranking dominants, suggesting that subordinates contribute relatively more when facing environmental challenges. We then test and confirm these predictions experimentally using the Asian burying beetle Nicrophorus nepalensis. Ultimately, we demonstrate how social rank modulates the relationships between environmental quality and cooperative and competitive behaviours, a topic crucial for understanding the evolution of complex societies.

Life histories determine divergent population trends for fishes under climate warming.

Most marine fish species express life-history changes across temperature gradients, such as faster growth, earlier maturation, and higher mortality at higher temperature. However, such climate-driven effects on life histories and population dynamics remain unassessed for most fishes. For 332 Indo-Pacific fishes, we show positive effects of temperature on body growth (but with decreasing asymptotic length), reproductive rates (including earlier age-at-maturation), and natural mortality for all species, with the effect strength varying among habitat-related species groups. Reef and demersal fishes are more sensitive to temperature changes than pelagic and bathydemersal fishes. Using a life table, we show that the combined changes of life histories upon increasing temperature tend to facilitate population growth for slow life-history populations, but reduce it for fast life-history ones. Within our data, lower proportions (25-30%) of slow life-history fishes but greater proportions of fast life-history fishes (42-60%) show declined population growth rates under 1 °C warming. Together, these findings suggest prioritizing sustainable management for fast life-history species.

Antagonistic effects of intraspecific cooperation and interspecific competition on thermal performance.

Understanding how climate-mediated biotic interactions shape thermal niche width is critical in an era of global change. Yet, most previous work on thermal niches has ignored detailed mechanistic information about the relationship between temperature and organismal performance, which can be described by a thermal performance curve. Here, we develop a model that predicts the width of thermal performance curves will be narrower in the presence of interspecific competitors, causing a species' optimal breeding temperature to diverge from that of its competitor. We test this prediction in the Asian burying beetle Nicrophorus nepalensis, confirming that the divergence in actual and optimal breeding temperatures is the result of competition with their primary competitor, blowflies. However, we further show that intraspecific cooperation enables beetles to outcompete blowflies by recovering their optimal breeding temperature. Ultimately, linking abiotic factors and biotic interactions on niche width will be critical for understanding species-specific responses to climate change.

Insects, reptiles and many other animals are often referred to as being 'cold-blooded' because, unlike mammals and birds, their body temperature fluctuates with the temperature of their surrounding environment. As a result, many cold-blooded animals are very sensitive to changes in local climate. Environmental factors, such as temperature and precipitation, as well biotic factors, such as two species competing for food or the presence of a predator, may influence how well an animal performs at different temperatures. However, few studies have examined how both environmental and biotic factors affect the range of temperatures in which a cold-blooded animal is able to survive and reproduce. When Asian burying beetles reproduce, they lay their eggs around buried animal carcasses that can provide food for their offspring. Previous studies have found that individual burying beetles can cooperate with each other to defend themselves against their main competitor, blowflies, which also lay their eggs on animal carcasses. Here, Tsai et al. used mathematical and experimental approaches to study how blowflies affect the range of temperatures in which burying beetles are able to live under different environmental conditions. The experiments showed that when blowflies were present, the range of temperatures that burying beetles were able to survive and reproduce in was smaller. Furthermore, the optimal temperature for the burying beetles to live in shifted back, away from that of their competitor. Larger groups of burying beetles were able to survive and reproduce in a greater range of temperatures than smaller groups, even when blowflies were present. This suggests that increasing the amount bury beetles cooperate with each other may make them more resilient to changes in temperature. The Earth is currently experiencing a period of climate change and therefore it is important to understand how different species of animals may respond to to changing temperatures. These findings reinforce the idea that even a small change in temperature may lead to changes in how different species interact with each other, which in turn influences the ecosystem in which they live.

Author Correction: Locally-adapted reproductive photoperiodism determines population vulnerability to climate change in burying beetles.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Complex signals alter recognition accuracy and conspecific acceptance thresholds.

Many aspects of behaviour depend on recognition, but accurate recognition is difficult because the traits used for recognition often overlap. For example, brood parasitic birds mimic host eggs, so it is challenging for hosts to discriminate between their own eggs and parasitic eggs. Complex signals that occur in multiple sensory modalities or involve multiple signal components are thought to facilitate accurate recognition. However, we lack models that explore the effect of complex signals on the evolution of recognition systems. Here, we use individual-based models with a genetic algorithm to test how complex signals influence recognition thresholds, signaller phenotypes and receiver responses. The model has three main results. First, complex signals lead to more accurate recognition than simple signals. Second, when two signals provide different amounts of information, receivers will rely on the more informative signal to make recognition decisions and may ignore the less informative signal. As a result, the particular traits used for recognition change over evolutionary time as sender and receiver phenotypes evolve. Third, complex signals are more likely to evolve when recognition errors are high cost than when errors are low cost. Overall, redundant, complex signals are an evolutionarily stable mechanism to reduce recognition errors. This article is part of the theme issue 'Signal detection theory in recognition systems: from evolving models to experimental tests'.

Locally-adapted reproductive photoperiodism determines population vulnerability to climate change in burying beetles.

Understanding how phenotypic traits vary among populations inhabiting different environments is critical for predicting a species' vulnerability to climate change. Yet, little is known about the key functional traits that determine the distribution of populations and the main mechanisms-phenotypic plasticity vs. local adaptation-underlying intraspecific functional trait variation. Using the Asian burying beetle Nicrophorus nepalensis, we demonstrate that mountain ranges differing in elevation and latitude offer unique thermal environments in which two functional traits-thermal tolerance and reproductive photoperiodism-interact to shape breeding phenology. We show that populations on different mountain ranges maintain similar thermal tolerances, but differ in reproductive photoperiodism. Through common garden and reciprocal transplant experiments, we confirm that reproductive photoperiodism is locally adapted and not phenotypically plastic. Accordingly, year-round breeding populations on mountains of intermediate elevation are likely to be most susceptible to future warming because maladaptation occurs when beetles try to breed at warmer temperatures.

A chemically triggered transition from conflict to cooperation in burying beetles.

Although interspecific competition has long been recognised as a major driver of trait divergence and adaptive evolution, relatively little effort has focused on how it influences the evolution of intraspecific cooperation. Here we identify the mechanism by which the perceived pressure of interspecific competition influences the transition from intraspecific conflict to cooperation in a facultative cooperatively breeding species, the Asian burying beetle Nicrophorus nepalensis. We not only found that beetles are more cooperative at carcasses when blowfly maggots have begun to digest the tissue, but that this social cooperation appears to be triggered by a single chemical cue - dimethyl disulfide (DMDS) - emitted from carcasses consumed by blowflies, but not from control carcasses lacking blowflies. Our results provide experimental evidence that interspecific competition promotes the transition from intraspecific conflict to cooperation in N. nepalensis via a surprisingly simple social chemical cue that is a reliable indicator of resource competition between species.

A continuum of biological adaptations to environmental fluctuation.

Bet-hedging-a strategy that reduces fitness variance at the expense of lower mean fitness among different generations-is thought to evolve as a biological adaptation to environmental unpredictability. Despite widespread use of the bet-hedging concept, most theoretical treatments have largely made unrealistic demographic assumptions, such as non-overlapping generations and fixed or infinite population sizes. Here, we extend the concept to consider overlapping generations by defining bet-hedging as a strategy with lower variance and mean per capita growth rate across different environments. We also define an opposing strategy-the rising-tide-that has higher mean but also higher variance in per capita growth. These alternative strategies lie along a continuum of biological adaptions to environmental fluctuation. Using stochastic Lotka-Volterra models to explore the evolution of the rising-tide versus bet-hedging strategies, we show that both the mean environmental conditions and the temporal scales of their fluctuations, as well as whether population dynamics are discrete or continuous, are crucial in shaping the type of strategy that evolves in fluctuating environments. Our model demonstrates that there are likely to be a wide range of ways that organisms with overlapping generations respond to environmental unpredictability beyond the classic bet-hedging concept.

Artificial intelligence reveals environmental constraints on colour diversity in insects.

Explaining colour variation among animals at broad geographic scales remains challenging. Here we demonstrate how deep learning-a form of artificial intelligence-can reveal subtle but robust patterns of colour feature variation along an ecological gradient, as well as help identify the underlying mechanisms generating this biogeographic pattern. Using over 20,000 images with precise GPS locality information belonging to nearly 2,000 moth species from Taiwan, our deep learning model generates a 2048-dimension feature vector that accurately predicts each species' mean elevation based on colour and shape features. Using this multidimensional feature vector, we find that within-assemblage image feature variation is smaller in high elevation assemblages. Structural equation modeling suggests that this reduced image feature diversity is likely the result of colder environments selecting for darker colouration, which limits the colour diversity of assemblages at high elevations. Ultimately, with the help of deep learning, we will be able to explore the endless forms of natural morphological variation at unpreceded depths.

Nest predation predicts infanticide in a cooperatively breeding bird.

In cooperatively breeding species, social conflict is typically assumed to underlie destructive behaviours like infanticide. However, an untested alternative hypothesis in birds is that infanticide in the form of egg tossing may simply be a parental response to partial nest predation representing a life-history trade-off. We examined egg tossing behaviour in the colonial and cooperatively breeding grey-capped social weaver (Pseudonigrita arnaudi), a plural breeder in which pairs nest separately, often in the same tree. Using infrared nest cameras, we found that 78% of the tossing events from 2012 to 2017 were committed by parents, suggesting that social conflict is unlikely to be the main reason underlying egg tossing in this species. Instead, reductions in clutch size due to both natural and experimentally simulated predation induced parental egg tossing. Our study suggests that destructive behaviour in cooperatively breeding birds can be shaped by a variety of mechanisms beyond social conflict and that alternative hypotheses must be considered when studying the adaptive significance of infanticide in group-living species.

Contrasting forms of competition set elevational range limits of species.

How abiotic and biotic factors constrain distribution limits at the harsh and benign edges of species ranges is hotly debated, partly because macroecological experiments testing the proximate causes of distribution limits are scarce. It has long been recognized - at least since Darwin's On the Origin of Species - that a harsh climate strengthens competition and thus sets species range limits. Using thorough field manipulations along a large elevation gradient, we show the mechanisms by which temperature determines competition type, resulting in a transition from interference to exploitative competition from the lower to the upper elevation limits in burying beetles (Nicrophorus nepalensis). This transition is an example of Darwin's classic hypothesis that benign climates favor direct competition for highly accessible resources while harsh climates result in competition through resources of high rivalry. We propose that identifying the properties of these key resources will provide a more predictive framework to understand the interplay between biotic and abiotic factors in determining geographic range limits.

Multitasking and the evolution of optimal clutch size in fluctuating environments.

Adaptive studies of avian clutch size variation across environmental gradients have resulted in what has become known as the fecundity gradient paradox, the observation that clutch size typically decreases with increasing breeding season length along latitudinal gradients, but increases with increasing breeding season length along elevational gradients. These puzzling findings challenge the common belief that organisms should reduce their clutch size in favor of additional nesting attempts as the length of the breeding season increases, an approach typically described as a bet-hedging strategy. Here, we propose an alternative hypothesis-the multitasking hypothesis-and show that laying smaller clutches represents a multitasking strategy of switching between breeding and recovery from breeding. Both our individual-based and analytical models demonstrate that a small clutch size strategy is favored during shorter breeding seasons because less time and energy are wasted under the severe time constraints associated with breeding multiply within a season. Our model also shows that a within-generation bet-hedging strategy is not favored by natural selection, even under a high risk of predation and in long breeding seasons. Thus, saving time-wasting less time as a result of an inability to complete a breeding cycle at the end of breeding season-is likely to be the primary benefit favoring the evolution of small avian clutch sizes during short breeding seasons. We also synthesize the seasonality hypothesis (pronounced seasonality leads to larger clutch size) and clutch size-dependent predation hypothesis (larger clutch size causes higher predation risks) within our multitasking hypothesis to develop an integrative model to help resolve the paradox of contrasting patterns of clutch size along elevational and latitudinal gradients. Ultimately, our models provide a new perspective for understanding life-history evolution under fluctuating environments.

The ecology of cooperative breeding behaviour.

Ecology is a fundamental driving force for the evolutionary transition from solitary living to breeding cooperatively in groups. However, the fact that both benign and harsh, as well as stable and fluctuating, environments can favour the evolution of cooperative breeding behaviour constitutes a paradox of environmental quality and sociality. Here, we propose a new model - the dual benefits framework - for resolving this paradox. Our framework distinguishes between two categories of grouping benefits - resource defence benefits that derive from group-defended critical resources and collective action benefits that result from social cooperation among group members - and uses insider-outsider conflict theory to simultaneously consider the interests of current group members (insiders) and potential joiners (outsiders) in determining optimal group size. We argue that the different grouping benefits realised from resource defence and collective action profoundly affect insider-outsider conflict resolution, resulting in predictable differences in the per capita productivity, stable group size, kin structure and stability of the social group. We also suggest that different types of environmental variation (spatial vs. temporal) select for societies that form because of the different grouping benefits, thus helping to resolve the paradox of why cooperative breeding evolves in such different types of environments.

Fishing-induced changes in adult length are mediated by skipped-spawning.

Elucidating fishing effects on fish population dynamics is a critical step toward sustainable fisheries management. Despite previous studies that have suggested age or size truncation in exploited fish populations, other aspects of fishing effects on population demography, e.g., via altering life histories and density, have received less attention. Here, we investigated the fishing effects altering adult demography via shifting reproductive trade-offs in the iconic, overexploited, Pacific bluefin tuna Thunnus orientalis. We found that, contrary to our expectation, mean lengths of catch increased over time in longline fisheries. On the other hand, mean catch lengths for purse seine fisheries did not show such increasing trends. We hypothesized that the size-dependent energetic cost of the spawning migration and elevated fishing mortality on the spawning grounds potentially drive size-dependent skipped spawning for adult tuna, mediating the observed changes in the catch lengths. Using eco-genetic individual-based modeling, we demonstrated that fishing-induced evolution of skipped spawning and size truncation interacted to shape the observed temporal changes in mean catch lengths for tuna. Skipped spawning of the small adults led to increased mean catch lengths for the longline fisheries, while truncation of small adults by the purse seines could offset such a pattern. Our results highlight the eco-evolutionary dynamics of fishing effects on population demography and caution against using demographic traits as a basis for fisheries management of the Pacific bluefin tuna as well as other migratory species.