Authors: Marina Telonis-Scott, Zeinab Ali, Sandra Hangartner, Carla M Sgrò

Published in: Journal of Thermal Biology

Abstract

Heat shock proteins (Hsps) have long been candidates for ecological adaptation given their unequivocal role in mitigating cell damage from heat stress, but linking Hsps to heat tolerance has proven difficult given the complexity of thermal adaptation.

Experimental evolution has been utilized to examine direct and correlated responses to selection for increased heat tolerance in Drosophila, often focusing on the major Hsp family Hsp70 and/or the master regulator HSF as a selection response, but rarely on other aspects of the heat shock complex.

We examined Hsp70 and co-chaperone stv isoform transcript expression in Australian D. melanogaster lines selected for static heat tolerance, and observed a temporal and stv isoform specific, coordinated transcriptional selection response with Hsp70, suggesting that increased chaperone output accompanied increased heat tolerance. We hypothesize that the coordinated evolutionary response of Hsp70 and stv may have arisen as a correlated response resulting from a shared regulatory hierarchy.

Our work highlights the complexity and specificity of the heat shock response in D. melanogaster.

The selected lines examined also showed correlated responses for other measures of heat tolerance, and the coevolution of Hsp70 and stv provide new avenues to examine the common mechanisms underpinning direct and correlated phenotypic responses to selection for heat tolerance.

Citation

Telonis-Scott M, Ali Z, Hangartner S, Sgrò CM (2021) Temporal specific coevolution of Hsp70 and co-chaperone stv expression in Drosophila melanogaster under selection for heat tolerance. Journal of Thermal Biology PDF DOI

Authors: Adriana P Rebolledo, Carla M Sgrò, and Keyne Monro

Published in: Frontiers in Physiology

Abstract

Understanding links between thermal performance and environmental variation is necessary to predict organismal responses to climate change, and remains an ongoing challenge for ectotherms with complex life cycles.

Distinct life stages can differ in thermal sensitivity, experience different environmental conditions as development unfolds, and, because stages are by nature interdependent, environmental effects can carry over from one stage to affect performance at others. Thermal performance may therefore respond to carryover effects of prior thermal environments, yet detailed insights into the nature, strength, and direction of those responses are still lacking.

Here, in an aquatic ectotherm whose early planktonic stages (gametes, embryos, and larvae) govern adult abundances and dynamics, we explore the effects of prior thermal environments at fertilization and embryogenesis on thermal performance curves at the end of planktonic development. We factorially manipulate temperatures at fertilization and embryogenesis, then, for each combination of prior temperatures, measure thermal performance curves for survival of planktonic development (end of the larval stage) throughout the performance range.

By combining generalized linear mixed modeling with parametric bootstrapping, we formally estimate and compare curve descriptors (thermal optima, limits, and breadth) among prior environments, and reveal carryover effects of temperature at embryogenesis, but not fertilization, on thermal optima at completion of development. Specifically, thermal optima shifted to track temperature during embryogenesis, while thermal limits and breadth remained unchanged.

Our results argue that key aspects of thermal performance are shaped by prior thermal environment in early life, warranting further investigation of the possible mechanisms underpinning that response, and closer consideration of thermal carryover effects when predicting organismal responses to climate change.

Citation

Rebolledo AP, Sgrò CM, Monro K (2021) Thermal performance curves are shaped by prior thermal environment in early life. Frontiers in Physiology PDF DOI

Authors: Avishikta Chakraborty, Carla M Sgrò, and Christen K Mirth

Published in: Journal of Insect Physiology

Abstract

Body size is a key life-history trait that influences many aspects of an animal’s biology and is shaped by a variety of factors, both genetic and environmental. While we know that locally-adapted populations differ in the extent to which body size responds plastically to environmental conditions like diet, we have a limited understanding of what causes these differences. We hypothesized that populations could differ in the way body size responds to nutrition either by modulating growth rate, development time, feeding rate, or a combination of the above.

Using three locally-adapted populations of Drosophila melanogaster from along the east coast of Australia, we investigated body size plasticity across five different diets. We then assessed how these populations differed in feeding behaviour and developmental timing on each of the diets.

We observed population-specific plastic responses to nutrition for body size and feeding rate, but not development time. However, differences in feeding rate did not fully explain the differences in the way body size responded to diet.

Thus, we conclude that body size variation in locally-adapted populations is shaped by a combination of growth rate and feeding behaviour. This paves the way for further studies that explore how differences in the regulation of the genetic pathways that control feeding behaviour and growth rate contribute to population-specific responses of body size to diet.

The different ways in which plastic variation in body size can be generated across organisms.

Citation

Chakraborty A, Sgrò CM, Mirth CK (2021) The proximate sources of genetic variation in body size plasticity: The relative contributions of feeding behaviour and development in Drosophila melanogaster. Journal of Insect Physiology PDF DOI

Authors: Fhallon Ware-Gilmore, Carla M Sgrò, Zhiyong Xi, Heverton LC Dutra, Matthew J Jones, Katriona Shea, Matthew D Hall, Matthew B Thomas, and Elizabeth A McGraw

Published in: PloS Neglected Tropical Diseases

The yellow fever mosquito Aedes aegypti is the primary vector of many disease-causing viruses, including dengue, Zika, chikungunya, and yellow fever viruses. Image credit: Vaccines by Sanofi, via Flickr (public domain).

Abstract

The mosquito Aedes aegypti is the primary vector of many disease-causing viruses, including dengue (DENV), Zika, chikungunya, and yellow fever. As consequences of climate change, we expect an increase in both global mean temperatures and extreme climatic events. When temperatures fluctuate, mosquito vectors will be increasingly exposed to temperatures beyond their upper thermal limits.

Here, we examine how DENV infection alters Ae. aegypti thermotolerance by using a high-throughput physiological ‘knockdown’ assay modeled on studies in Drosophila. Such laboratory measures of thermal tolerance have previously been shown to accurately predict an insect’s distribution in the field.

We show that DENV infection increases thermal sensitivity, an effect that may ultimately limit the geographic range of the virus. We also show that the endosymbiotic bacterium Wolbachia pipientis, which is currently being released globally as a biological control agent, has a similar impact on thermal sensitivity in Ae. aegypti. Surprisingly, in the coinfected state, Wolbachia did not provide protection against DENV-associated effects on thermal tolerance, nor were the effects of the two infections additive. The latter suggests that the microbes may act by similar means, potentially through activation of shared immune pathways or energetic tradeoffs.

Models predicting future ranges of both virus transmission and Wolbachia’s efficacy following field release may wish to consider the effects these microbes have on host survival.

Citation

Ware-Gilmore F, Sgrò CM, Xi Z, Dutra HLC, Jones MJ, Shea K, Hall MD, Thomas MB, McGraw EA (2021) Microbes increase thermal sensitivity in the mosquito Aedes aegypti, with the potential to change disease distributions. PLoS Neglected Tropical Diseases PDF DOI

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

Published in: Biology Letters

Abstract

Natural populations are experiencing an increase in the occurrence of both thermal stress and disease outbreaks. How these two common stressors interact to determine host phenotypic shifts will be important for population persistence, yet a myriad different traits and pathways are a target of both stressors, making generalizable predictions difficult to obtain.

Here, using the host Daphnia magna and its bacterial pathogen Pasteuria ramosa, we tested how temperature and pathogen exposure interact to drive shifts in multivariate host phenotypes.

We found that these two stressors acted mostly independently to shape host phenotypic trajectories, with temperature driving a faster pace of life by favouring early development and increased intrinsic population growth rates, while pathogen exposure impacted reproductive potential through reductions in lifetime fecundity.

Studies focussed on extreme thermal stress are increasingly showing how pathogen exposure can severely hamper the thermal tolerance of a host. However, our results suggest that under milder thermal stress, and in terms of life-history traits, increases in temperature might not exacerbate the impact of pathogen exposure on host performance, and vice versa.

Citation

Hector TE, Sgrò CM, Hall MD (2021) Temperature and pathogen exposure act independently to drive host phenotypic trajectories. Biology Letters PDF DOI

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

Published in: Global Change Biology

Abstract

The frequency and severity of both extreme thermal events and disease outbreaks are predicted to continue to shift as a consequence of global change. As a result, species persistence will likely be increasingly dependent on the interaction between thermal stress and pathogen exposure.

Missing from the intersection between studies of infectious disease and thermal ecology, however, is the capacity for pathogen exposure to directly disrupt a host’s ability to cope with thermal stress. Common sources of variation in host thermal performance, which are likely to interact with infection, are also often unaccounted for when assessing either the vulnerability of species or the potential for disease spread during extreme thermal events.

Here, we describe how infection can directly alter host thermal limits, to a degree that exceeds the level of variation commonly seen across species large geographic distributions and that equals the detrimental impact of other ecologically relevant stressors. We then discuss various sources of heterogeneity within and between populations that are likely to be important in mediating the impact that infection has on variation in host thermal limits.

In doing so we highlight how infection is a widespread and important source of variation in host thermal performance, which will have implications for both the persistence and vulnerability of species and the dynamics and transmission of disease in a more thermally extreme world.

Citation

Hector TE, Sgrò CM, Hall MD (2021) Thermal limits in the face of infectious disease: How important are pathogens? Global Change Biology PDF DOI

Authors: Carly N Cook, Erik A Beever, Lindsey L Thurman, Laura M Thompson, John E Gross, Andrew R Whiteley, Adrienne B Nicotra, Jennifer A Szymanski, Carlos A Botero, Kimberly R Hall, Ary A Hoffmann, Gregor W Schuurman, and Carla M Sgrò

Published in: Evolutionary Applications

Abstract

There is an imperative for conservation practitioners to help biodiversity adapt to accelerating environmental change.

Evolutionary biologists are well-positioned to inform the development of evidence-based management strategies that support the adaptive capacity of species and ecosystems. Conservation practitioners increasingly accept that management practices must accommodate rapid environmental change, but harbour concerns about how to apply recommended changes to their management contexts. Given the interest from both conservation practitioners and evolutionary biologists in adjusting management practices, we believe there is an opportunity to accelerate the required changes by promoting closer collaboration between these two groups.

Left: A robust evidence base to support successful management practices, based on an incremental scaling up in spatial extent and ecological complexity. Right: Four elements involved in supporting effective knowledge exchange.

We highlight how evolutionary biologists can harness lessons from other disciplines about how to foster effective knowledge exchange to make a substantive contribution to the development of effective conservation practices. These lessons include the following:

1. recognizing why practitioners do and do not use scientific evidence
2. building an evidence base that will influence management decisions
3. translating theory into a format that conservation practitioners can use to inform management practices; and
4. developing strategies for effective knowledge exchange.

Although efforts will be required on both sides, we believe there are rewards for both practitioners and evolutionary biologists, not least of which is fostering practices to help support the long-term persistence of species.

Citation

Cook CN, Beever EA, Thurman LL, Thompson LM, Gross JE, Whiteley AR, Nicotra AB, Szymanski JA, Botero CA, Hall KR, Hoffmann AA, Schuurman GW, Sgrò CM (2021) Supporting the adaptive capacity of species through more effective knowledge exchange with conservation practitioners. Evolutionary Applications PDF DOI

Authors: Katrina McGuigan, Ary A Hoffmann, and Carla M Sgrò

Published in: Philosophical Transactions of The Royal Society B

Abstract

Transgenerational effects that are interpreted in terms of epigenetics have become an important research focus at a time when rapid environmental changes are occurring. These effects are usually interpreted as enhancing fitness extremely rapidly, without depending on the slower process of natural selection changing DNA-encoded (fixed) genetic variants in populations. Supporting evidence comes from a variety of sources, including environmental associations with epialleles, cross-generation responses of clonal material exposed to different environmental conditions, and altered patterns of methylation or frequency changes in epialleles across time.

Transgenerational environmental effects have been postulated to be larger than those associated with DNA-encoded genetic changes, based on (for instance) stronger associations between epialleles and environmental conditions. Yet environmental associations for fixed genetic differences may always be weak under polygenic models where multiple combinations of alleles can lead to the same evolutionary outcome. The ultimate currency of adaptation is fitness, and few transgenerational studies have robustly determined fitness effects, particularly when compared to fixed genetic variants.

Not all transgenerational modifications triggered by climate change will increase fitness: stressful conditions often trigger negative fitness effects across generations that can eliminate benefits. Epigenetic responses and other transgenerational effects will undoubtedly play a role in climate change adaptation, but further, well-designed, studies are required to test their importance relative to DNA-encoded changes.

This article is part of the theme issue ‘How does epigenetics influence the course of evolution?’

Citation

McGuigan K, Hoffmann AA, Sgrò CM (2021) How is epigenetics predicted to contribute to climate change adaptation? What evidence do we need? Philosophical Transactions of The Royal Society B PDF DOI

Authors: Belinda van Heerwaarden and Carla M Sgrò

Published in: Nature Communications

Abstract

Forecasting which species/ecosystems are most vulnerable to climate warming is essential to guide conservation strategies to minimize extinction.

Tropical/mid-latitude species are predicted to be most at risk as they live close to their upper critical thermal limits (CTLs). However, these assessments assume that upper CTL estimates, such as CTmax, are accurate predictors of vulnerability and ignore the potential for evolution to ameliorate temperature increases.

Here, we use experimental evolution to assess extinction risk and adaptation in tropical and widespread Drosophila species.

We find tropical species succumb to extinction before widespread species. Male fertility thermal limits, which are much lower than CTmax, are better predictors of species’ current distributions and extinction in the laboratory.

We find little evidence of adaptive responses to warming in any species. These results suggest that species are living closer to their upper thermal limits than currently presumed and evolution/plasticity are unlikely to rescue populations from extinction.

Citation

van Heerwaarden B, Sgrò CM (2021) Male fertility thermal limits predict vulnerability to climate warming. Nature Communications PDF DOI

Authors: Ary A Hoffmann, Andrew R Weeks, and Carla M Sgrò

Published in: Cell

Abstract

By investigating how past selection has affected allele frequencies across space, genomic tools are providing new insights into adaptive evolutionary processes.

Now researchers are considering how this genomic information can be used to predict the future vulnerability of species under climate change.

Genomic vulnerability assessments show promise, but challenges remain.

Citation

Hoffmann AA, Weeks AR, Sgrò CM (2021) Opportunities and challenges in assessing climate change vulnerability through genomics. Cell PDF DOI