Heat tolerance predicts the importance of species interaction effects as the climate changes

Few studies have quantified the relative importance of direct effects of climate change on communities versus indirect effects that are mediated thorough species interactions, and the limited evidence is conflicting. Trait-based approaches have been popular in studies of climate change, but can they be used to estimate direct versus indirect effects? At the species level, thermal tolerance is a trait that is often used to predict winners and losers under scenarios of climate change. But thermal tolerance might also inform when species interactions are likely to be important because only subsets of species will be able to exploit the available warmer climatic niche space, and competition may intensify in the remaining, compressed cooler climatic niche space. Here, we explore the relative roles of the direct effects of temperature change and indirect effects of species interactions on forest ant communities that were heated as part of a large-scale climate manipulation at high-A nd low-latitude sites in eastern North America. Overall, we found mixed support for the importance of negative species interactions (competition), but found that the magnitude of these interaction effects was predictable based on the heat tolerance of the focal species. Forager abundance and nest site occupancy of heat-intolerant species were more often influenced by negative interactions with other species than by direct effects of temperature. Our findings suggest that measures of species-specific heat tolerance may roughly predict when species interactions will influence responses to global climate change

Thermal reactionomes reveal divergent responses to thermal extremes in warm and cool-climate ant species

Background: The distributions of species and their responses to climate change are in part determined by their thermal tolerances. However, little is known about how thermal tolerance evolves. To test whether evolutionary extension of thermal limits is accomplished through enhanced cellular stress response (enhanced response), constitutively elevated expression of protective genes (genetic assimilation) or a shift from damage resistance to passive mechanisms of thermal stability (tolerance), we conducted an analysis of the reactionome: the reaction norm for all genes in an organism\u27s transcriptome measured across an experimental gradient. We characterized thermal reactionomes of two common ant species in the eastern U.S, the northern cool-climate Aphaenogaster picea and the southern warm-climate Aphaenogaster carolinensis, across 12 temperatures that spanned their entire thermal breadth. Results: We found that at least 2 % of all genes changed expression with temperature. The majority of upregulation was specific to exposure to low temperatures. The cool-adapted A. picea induced expression of more genes in response to extreme temperatures than did A. carolinensis, consistent with the enhanced response hypothesis. In contrast, under high temperatures the warm-adapted A. carolinensis downregulated many of the genes upregulated in A. picea, and required more extreme temperatures to induce down-regulation in gene expression, consistent with the tolerance hypothesis. We found no evidence for a trade-off between constitutive and inducible gene expression as predicted by the genetic assimilation hypothesis. Conclusions: These results suggest that increases in upper thermal limits may require an evolutionary shift in response mechanism away from damage repair toward tolerance and prevention

Linking physiology and biogeography: Disentangling the constraints on the distributions of ant species

Understanding the factors that limit the distribution of species is at the core of ecological and biogeographical research, and is critical if we are to predict the responses of key ecosystem components to ongoing climatic changes. My doctoral research seeks to provide an understanding of how thermal physiology influences species’ distributions and better define the mechanisms underlying geographic variation in biodiversity. By using natural temperature gradients (both elevational and latitudinal) and coupling controlled laboratory experiments with field observations and null modeling approaches, I was able to document the role of inter-specific variation in thermal physiology and, more interesting, inter-population variation in thermal physiology, in shaping the distribution of diversity on a warming planet. I determined that species’ density and distributions are shaped by both biotic and abiotic factors, but that the influence of these factors is geographically-dependent. I further examined the role of temperature by determining how different rates of warming affect thermal physiology and might provide insight into separate aspects of an organism’s life history and its accompanying coping mechanisms. Finally, I used a common garden experiment and phylogenetic analyses to determine to what extent ecological and evolutionary forces play a role in shaping the thermal niche. I found patterns suggestive of local adaptation and no evidence for lab acclimation, suggesting that some species may have limited acclimation ability and therefore will be more susceptible to climate warming. This dissertation suggests that variation in thermal physiology within and among species is important in understanding the factors that shape diversity and how species will be distributed now, and in the future

Field_versus_F2_CTmax

This dataset contains 4 columns, including “colonyID”, “ctmax”, “generation”, and “population”. Each row of the dataset represents the response of an individual worker acorn ant. colonyID – a unique identifier for each acorn ant colony; multiple individual workers were tested from the same colony. ctmax – a continuous numeric variable describing the value for the critical thermal maximum in degrees Celsius. generation – a categorical variable describing whether the data come from the field-caught generation or the F2 (lab-born) generation. population – a categorical variable describing whether the ants originated from a rural or an urban site

F2_CTmax_CTmin

This dataset contains 5 columns, including “colonyID”, “date.tt”, “thermal.tolerance.trait”, “thermal.tolerance”, and “cross”. Each row of the dataset represents the response of an individual worker acorn ant. colonyID – a unique identifier for each acorn ant colony; multiple individual workers were tested from the same colony. date.tt – the date (month/day/year) that the thermal tolerance assessment was conducted. thermal.tolerance.trait – a categorical variable describing whether the critical thermal minimum (ctmin) or critical thermal maximum (ctmax) was assessed on the individual worker ant. thermal.tolerance – a continuous numeric value describing either the ctmax or ctmin. Values are presented in units of degrees Celsius. cross – a categorical variable describing the type of cross used to generate the F2 acorn ant workers. This variable has 4 levels, including “rur-rur” which describes a cross where both parents are from rural populations; “urb-urb” which describes a cross where both parents are from urban populations; “rur-urb” which describes a cross where the mother was from a rural population and the father from an urban population; and “urb-rur” which describes a cross where the mother was from an urban population and the father was from a rural population

Field_versus_F2_CTmin

This dataset contains 4 columns, including “colonyID”, “ctmax”, “generation”, and “population”. Each row of the dataset represents the response of an individual worker acorn ant. colonyID – a unique identifier for each acorn ant colony; multiple individual workers were tested from the same colony. ctmin – a continuous numeric variable describing the value for the critical thermal minimum in degrees Celsius. generation – a categorical variable describing whether the data come from the field-caught generation or the F2 (lab-born) generation. population – a categorical variable describing whether the ants originated from a rural or an urban site

Data from: Evolution of thermal tolerance and its fitness consequences: parallel and non-parallel responses to urban heat islands across three cities

The question of parallel evolution—what causes it, and how common it is—has long captured the interest of evolutionary biologists. Widespread urban development over the last century has driven rapid evolutionary responses on contemporary timescales, presenting a unique opportunity to test the predictability and parallelism of evolutionary change. Here we examine rapid urban evolution in an acorn-dwelling ant species, focusing on the urban heat island signal and the ant’s tolerance of these altered urban temperature regimes. Using a common-garden experimental design with acorn ant colonies collected from urban and rural populations in three cities and reared under five temperature treatments in the laboratory, we assessed plastic and evolutionary shifts in the heat and cold tolerance of F1 offspring worker ants. In two of three cities, we found evolved losses of cold tolerance, and compression of thermal tolerance breadth. Results for heat tolerance were more complex: in one city, we found evidence of simple evolved shifts in heat tolerance in urban populations, though in another, the difference in urban and rural population heat tolerance depended on laboratory rearing temperature, and only became weakly apparent at the warmest rearing temperatures. The shifts in tolerance appeared to be adaptive, as our analysis of the fitness consequences of warming revealed that while urban populations produced more sexual reproductives under warmer laboratory rearing temperatures, rural populations produced fewer. Patterns of natural selection on thermal tolerances supported our findings of fitness tradeoffs and local adaptation across urban and rural acorn ant populations, as selection on thermal tolerance acted in opposite directions between the warmest and coldest rearing temperatures. Our study provides mixed support for parallel evolution of thermal tolerance under urban temperature rise