Pathogen exposure reduces sexual dimorphism in a host’s upper thermal limits

Authors: Tess Laidlaw, Tobias E Hector, Carla M. Sgrò, and Matthew D Hall

Published in: Ecology and Evolution

Abstract

The climate is warming at an unprecedented rate, pushing many species toward and beyond the upper temperatures at which they can survive. Global change is also leading to dramatic shifts in the distribution of pathogens. As a result, upper thermal limits and susceptibility to infection should be key determinants of whether populations continue to persist, or instead go extinct. Within a population, however, individuals vary in both their resistance to both heat stress and infection, and their contributions to vital growth rates. No more so is this true than for males and females. Each sex often varies in their response to pathogen exposure, thermal tolerances, and particularly their influence on population growth, owing to the higher parental investment that females typically make in their offspring. To date, the interplay between host sex, infection, and upper thermal limits has been neglected.

Here, we explore the response of male and female Daphnia to bacterial infection and static heat stress.

We find that female Daphnia, when uninfected, are much more resistant to static heat stress than males, but that infection negates any advantage that females are afforded. We discuss how the capacity of a population to cope with multiple stressors may be underestimated unless both sexes are considered simultaneously.

Citation

Laidlaw T, Hector TE, Sgrò CM, Hall MD (2020) Pathogen exposure reduces sexual dimorphism in a host’s upper thermal limits. Ecology and Evolution PDF DOI

Genetic covariances promote climatic adaptation in Australian Drosophila

Authors: Sandra Hangartner, Clementine Lasne, Carla M Sgrò, Tim Connallon, and Keyne Monro

Published in: Evolution

Abstract

Evolutionary potential for adaptation hinges upon the orientation of genetic variation for traits under selection, captured by the additive genetic variance‐covariance matrix (G), as well as the evolutionary stability of G. Yet studies that assess both the stability of G and its alignment with selection are extraordinarily rare.

We evaluated the stability of G in three Drosophila melanogaster populations that have adapted to local climatic conditions along a latitudinal cline. We estimated population- and sex-specific G matrices for wing size and three climatic stress-resistance traits that diverge adaptively along the cline. To determine how G affects evolutionary potential within these populations, we used simulations to quantify how well G aligns with the direction of trait divergence along the cline (as a proxy for the direction of local selection) and how genetic covariances between traits and sexes influence this alignment.

We found that G was stable across the cline, showing no significant divergence overall, or in sex-specific subcomponents, among populations. G also aligned well with the direction of clinal divergence, with genetic covariances strongly elevating evolutionary potential for adaptation to climatic extremes. These results suggest that genetic covariances between both traits and sexes should significantly boost evolutionary responses to environmental change.

Citation

Hangartner S, Lasne C, Sgrò CM, Connallon T, Monro K (2020) Genetic covariances promote climatic adaptation in Australian Drosophila. Evolution PDF DOI

Interacting with change: Diet mediates how larvae respond to their thermal environment

Authors: Teresa C Kutz, Carla M. Sgrò, and Christen K Mirth

Published in: Functional Ecology

Abstract

Temperature and nutrition are amongst the most common environmental challenges faced by organisms and will become increasingly so with ongoing climate change. While we have learnt a great deal about how temperature and nutrition affect life‐history traits on their own, we know very little about their combined effect on animal performance. Given that animals in the wild are likely to experience changes in both their thermal and nutritional conditions, we need to understand how interactions between these conditions shape an animal’s response if we hope to mitigate the effects of environmental change.

In the present research, we investigated the combined effects of nutrition and temperature on key life‐history traits in Drosophila melanogaster. Using nutritional geometry, developing larvae were exposed to a range of diets varying in their protein and carbohydrate content and to one of two developmental temperature regimes (25°C and 28°C). We then examined key life-history traits: development time, viability, and two estimates of body size — wing and femur size.

We found that developmental temperature significantly changed the response to nutrition for all traits. Increased temperature led to more restricted trait optima for all traits and exacerbated the negative effects of carbohydrate-rich diets, resulting in harsher trade-offs between life-history traits. For example, at 25°C there were more diets that led to high viability, fast development and large body size than at 28°C. However, for the diets that produced the best outcomes for each trait, temperature had less of an effect.

These findings highlight the importance of studying the effects of combined stressors when assessing animals’ responses to changing environmental conditions.

Citation

Kutz TC, Sgrò CM, Mirth CK (2019) Interacting with change: Diet mediates how larvae respond to their thermal environment. Functional Ecology PDF DOI

Comparing thermal performance curves across traits: how consistent are they?

Authors: Vanessa Kellermann, Steven L Chown, Mads Fristrup Schou, Ian Aitkenhead, Charlene Janion-Scheepers, Allannah Clemson, Marina Telonis Scott, and Carla M. Sgrò

Published in: Journal of Experimental Biology

Abstract

Thermal performance curves (TPCs) are intended to approximate the relationship between temperature and fitness, and are commonly integrated into species distributional models for understanding climate change responses. However, TPCs may vary across traits because selection and environmental sensitivity (plasticity) differ across traits or because the timing and duration of the temperature exposure, here termed time scale, may alter trait variation. Yet, the extent to which TPCs vary temporally and across traits is rarely considered in assessments of climate change responses.

Using a common garden approach, we estimated TPCs for standard metabolic rate (SMR), and activity in Drosophila melanogaster at three test temperatures (16, 25 and 30°C), using flies from each of six developmental temperatures (16, 18, 20, 25, 28 and 30°C). We examined the effects of time scale of temperature exposure (minutes/hours versus days/weeks) in altering TPC shape and position, and commonly used descriptors of the TPC: thermal optimum (Topt), thermal limits (Tmin and Tmax) and thermal breadth (Tbr). In addition, we collated previously published estimates of TPCs for fecundity and egg-to-adult viability in D. melanogaster.

We found that the descriptors of the TPCs varied across traits (egg-to-adult viability, SMR, activity and fecundity), but variation in TPCs within these traits was small across studies when measured at the same time scales. The time scale at which traits were measured contributed to greater variation in TPCs than the observed variance across traits, although the relative importance of time scale differed depending on the trait (activity versus fecundity). Variation in the TPC across traits and time scales suggests that TPCs using single traits may not be an accurate predictor of fitness and thermal adaptation across environments.

Citation

Kellermann V, Chown SL, Schou MF, Aitkenhead I, Janion-Scheepers C, Clemson A, Scott MT, Sgrò CM (2019) Comparing thermal performance curves across traits: how consistent are they? Journal of Experimental Biology PDF DOI

Pathogen exposure disrupts an organism’s ability to cope with thermal stress

Authors: Tobias E Hector, Carla M. Sgrò, and Matthew D Hall

Published in: Global Change Biology

Abstract

As a result of global climate change, species are experiencing an escalation in the severity and regularity of extreme thermal events. With patterns of disease distribution and transmission predicted to undergo considerable shifts in the coming years, the interplay between temperature and pathogen exposure will likely determine the capacity of a population to persist under the dual threat of global change and infectious disease.

In this study, we investigated how exposure to a pathogen affects an individual’s ability to cope with extreme temperatures. Using experimental infections of Daphnia magna with its obligate bacterial pathogen Pasteuria ramosa, we measured upper thermal limits of multiple host and pathogen genotype combinations across the dynamic process of infection and under various forms (static and ramping) of thermal stress.

We find that pathogens substantially limit the thermal tolerance of their host, with the reduction in upper thermal limits on par with the breadth of variation seen across similar species entire geographical ranges. The precise magnitude of any reduction, however, was specific to the host and pathogen genotype combination. In addition, as thermal ramping rate slowed, upper thermal limits of both healthy and infected individuals were reduced.

Our results suggest that the capacity of a population to evolve new thermal limits, when also faced with the threat of infection, will depend not only on a host’s genetic variability in warmer environments, but also on the frequency of host and pathogen genotypes. We suggest that pathogen‐induced alterations of host thermal performance should be taken into account when assessing the resilience of any population and its potential for adaptation to global change.

Citation

Hector TE, Sgrò CM, Hall MD (2019) Pathogen exposure disrupts an organism’s ability to cope with thermal stress. Global Change Biology PDF DOI

Conservation practitioners’ understanding of how to manage evolutionary processes

Authors: Carly N Cook and Carla M. Sgrò

Published in: Conservation Biology

Abstract

Both academics and practitioners consider a lack of knowledge about evolutionary theory to be a general barrier to effectively managing genetic diversity. However, it is challenging to judge practitioners’ level of understanding and how this influences their management decisions. Knowledge built through experience may be difficult for practitioners to articulate, but could nonetheless result in appropriate management strategies. To date, researchers have assessed only the explicit (formal) knowledge practitioners have of evolutionary concepts.

To explore practitioners’ understanding of evolutionary concepts, it is necessary to consider how they might apply explicit and implicit knowledge to their management decisions. Using an online survey, we asked Australian practitioners to respond to 2 common management scenarios in which there is strong evidence that managing genetic diversity can improve outcomes: managing small, isolated populations and sourcing seeds for restoration projects.

In describing their approach to these scenarios, practitioners demonstrated a stronger understanding of the effective management of genetic diversity than the definitions of the relevant concepts. However, their management of genetic diversity within small populations was closer to best practice than for restoration projects. Moreover, the risks practitioners described in implementing best practice management were more likely to affect their approach to restoration than translocation projects.

These findings provide evidence that strategies to build the capacity of practitioners to manage genetic diversity should focus on realistic management scenarios. Given that practitioners recognize the importance of adapting their practices and the strong evidence for the benefits of actively managing genetic diversity, there is hope that better engagement by evolutionary biologists with practitioners could facilitate significant shifts toward evolutionarily enlightened management.

Citation

Cook CN, Sgrò CM (2019) Conservation practitioners’ understanding of how to manage evolutionary processes. Conservation Biology PDF DOI

Genomic changes associated with adaptation to arid environments in cactophilic Drosophila species

Authors: Rahul V Rane, Stephen L Pearce, Fang Li, Chris Coppin, Michele Schiffer, Jennifer Shirriffs, Carla M Sgrò, Philippa C Griffin, Goujie Zhang, Siu F Lee, Ary A Hoffmann, and John G Oakeshott

Published in: BMC Genomics

Abstract

Insights into the genetic capacities of species to adapt to future climate change can be gained by using comparative genomic and transcriptomic data to reconstruct the genetic changes associated with such adaptations in the past.

Here we investigate the genetic changes associated with adaptation to arid environments, specifically climatic extremes and new cactus hosts, through such an analysis of five repleta group Drosophila species.

We find disproportionately high rates of gene gains in internal branches in the species’ phylogeny where cactus use and subsequently cactus specialisation and high heat and desiccation tolerance evolved. The terminal branch leading to the most heat and desiccation resistant species, Drosophila aldrichi, also shows disproportionately high rates of both gene gains and positive selection. Several Gene Ontology terms related to metabolism were enriched in gene gain events in lineages where cactus use was evolving, while some regulatory and developmental genes were strongly selected in the Drosophila aldrichi branch. Transcriptomic analysis of flies subjected to sublethal heat shocks showed many more downregulation responses to the stress in a heat sensitive versus heat resistant species, confirming the existence of widespread regulatory as well as structural changes in the species’ differing adaptations. Gene Ontology terms related to metabolism were enriched in the differentially expressed genes in the resistant species while terms related to stress response were over-represented in the sensitive one.

Adaptations to new cactus hosts and hot desiccating environments were associated with periods of accelerated evolutionary change in diverse biochemistries. The hundreds of genes involved suggest adaptations of this sort would be difficult to achieve in the timeframes projected for anthropogenic climate change.

Citation

Rane RV, Pearce SL, Li F, Coppin C, Schiffer M, Shirriffs J, Sgrò CM, Griffin PC, Zhang G, Lee SF, Hoffmann AA, Oakeshott JG (2019) Genomic changes associated with adaptation to arid environments in cactophilic Drosophila species, BMC Genomics. PDF DOI

Poor understanding of evolutionary theory is a barrier to effective conservation management

Authors: Carly N Cook and Carla M. Sgrò

Published in: Conservation Letters

Abstract

Despite increasing recognition that integrating evolutionary theory into conservation decisions can achieve better long-term outcomes, there has been little progress adapting management strategies. A commonly hypothesized barrier to better integration is poor understanding of evolutionary biology among conservation practitioners.

To assess this claim, we surveyed conservation practitioners to determine their understanding of evolutionary concepts.

We found that most practitioners had a good understanding of general concepts (evolution and genetic diversity), but a much poorer understanding of other relevant concepts.

These findings suggest that knowledge is limiting the ability of conservation practitioners to effectively manage evolutionary processes. Encouragingly, practitioners educated in evolutionary biology and population genetics had a better understanding, suggesting focused training is important. However, better integration of evolutionary theory will require that evolutionary biologists develop a culture of knowledge exchange, actively engaging practitioners to improve management. Otherwise, our findings suggest it is unlikely practitioners will be able to adapt their practices.

Citation

Cook CN, Sgrò CM (2019) Poor understanding of evolutionary theory is a barrier to effective conservation management. Conservation Letters PDF DOI

Quantifying the relative contributions of the X chromosome, autosomes, and mitochondrial genome to local adaptation

Authors: Clementine Lasne, Belinda van Heerwaarden, Carla M Sgrò, and Tim Connallon

Published in: Evolution

Abstract

During local adaptation with gene flow, some regions of the genome are inherently more responsive to selection than others.

Recent theory predicts that X‐linked genes should disproportionately contribute to local adaptation relative to other genomic regions, yet this prediction remains to be tested.

We carried out a multigeneration crossing scheme, using two cline‐end populations of Drosophila melanogaster, to estimate the relative contributions of the X chromosome, autosomes, and mitochondrial genome to divergence in four traits involved in local adaptation (wing size, resistance to heat, desiccation, and starvation stresses).

We found that the mitochondrial genome and autosomes contributed significantly to clinal divergence in three of the four traits. In contrast, the X made no significant contribution to divergence in these traits.

Given the small size of the mitochondrial genome, our results indicate that it plays a surprisingly large role in clinal adaptation. In contrast, the X, which represents roughly 20% of the Drosophila genome, contributes negligibly—a pattern that conflicts with theoretical predictions. These patterns reinforce recent work implying a central role of mitochondria in climatic adaptation, and suggest that different genomic regions may play fundamentally different roles in processes of divergence with gene flow.

Citation

Lasne C, Heerwaarden B, Sgrò CM, Connallon T (2019) Quantifying the relative contributions of the X chromosome, autosomes, and mitochondrial genome to local adaptation, Evolution PDF DOI

How does parental environment influence the potential for adaptation to global change?

Authors: Evatt Chirgwin, Dustin J. Marshall, Carla M. Sgrò, and Keyne Monro

Published in: Proceedings of the Royal Society B: Biological Sciences

Abstract

Parental environments are regularly shown to alter the mean fitness of offspring, but their impacts on the genetic variation for fitness, which predicts adaptive capacity and is also measured on offspring, are unclear. Consequently, how parental environments mediate adaptation to environmental stressors, like those accompanying global change, is largely unknown.

Here, using an ecologically important marine tubeworm in a quantitative-genetic breeding design, we tested how parental exposure to projected ocean warming alters the mean survival, and genetic variation for survival, of offspring during their most vulnerable life stage under current and projected temperatures.

Offspring survival was higher when parent and offspring temperatures matched. Across offspring temperatures, parental exposure to warming altered the distribution of additive genetic variance for survival, making it covary across current and projected temperatures in a way that may aid adaptation to future warming. Parental exposure to warming also amplified nonadditive genetic variance for survival, suggesting that compatibilities between parental genomes may grow increasingly important under future warming.

Our study shows that parental environments potentially have broader-ranging effects on adaptive capacity than currently appreciated, not only mitigating the negative impacts of global change but also reshaping the raw fuel for evolutionary responses to it.

Citation

Chirgwin E, Marshall DJ, Sgrò CM, Monro K (2018) How does parental environment influence the potential for adaptation to global change? Proceedings of the Royal Society B: Biological SciencesPDF DOI