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

Authors: Dana M Bergstrom, Barbara C Wienecke, John van den Hoff, Lesley Hughes, David B Lindenmayer, Tracy D Ainsworth, Christopher M Baker, Lucie Bland, David MJS Bowman, Shaun T Brooks, Josep G Canadell, Andrew J Constable, Katherine A Dafforn, Michael H Depledge, Catherine R Dickson, Norman C Duke, Kate J Helmstedt, Andrés Holz, Craig R Johnson, Melodie A McGeoch, Jessica Melbourne-Thomas, Rachel Morgain, Emily Nicholson, Suzanne M Prober, Ben Raymond, Euan G Ritchie, Sharon A Robinson, Katinka X Ruthrof, Samantha A Setterfield, Carla M Sgrò, Jonathan S Stark, Toby Travers, Rowan Trebilco, Delphi FL Ward, Glenda M Wardle, Kristen J Williams, Phillip J Zylstra, and Justine D Shaw

Published in: Global Change Biology

Abstract

Globally, collapse of ecosystems — potentially irreversible change to ecosystem structure, composition and function — imperils biodiversity, human health and well-being.

We examine the current state and recent trajectories of 19 ecosystems, spanning 58° of latitude across 7.7 million km², from Australia’s coral reefs to terrestrial Antarctica.

Pressures from global climate change and regional human impacts, occurring as chronic ‘presses’ and/or acute ‘pulses’, drive ecosystem collapse. Ecosystem responses to 5–17 pressures were categorised as four collapse profiles — abrupt, smooth, stepped and fluctuating. The manifestation of widespread ecosystem collapse is a stark warning of the necessity to take action.

We present a three-step assessment and management framework (3As Pathway Awareness, Anticipation and Action) to aid strategic and effective mitigation to alleviate further degradation to help secure our future.

Citation

Bergstrom DM, Wienecke BC, Hoff J, Hughes L, Lindenmayer DB, Ainsworth TD, Baker CM, Bland L, Bowman DMJS, Brooks ST, Canadell JG, Constable AJ, Dafforn KA, Depledge MH, Dickson CR, Duke NC, Helmstedt KJ, Holz A, Johnson CR, McGeoch MA, Melbourne‐Thomas J, Morgain R, Nicholson E, Prober SM, Raymond B, Ritchie EG, Robinson SA, Ruthrof KX, Setterfield SA, Sgrò CM, Stark JS, Travers T, Trebilco R, Ward DFL, Wardle GM, Williams KJ, Zylstra PJ, Shaw JD (2021) Combating ecosystem collapse from the tropics to the Antarctic. Global Change Biology PDF DOI

Authors: Brooke Zanco, Christen K Mirth, Carla M Sgrò, and Matthew DW Piper

Published in: eLife

Abstract

Diet plays a significant role in maintaining lifelong health. In particular, lowering the dietary protein: carbohydrate ratio can improve lifespan. This has been interpreted as a direct effect of these macronutrients on physiology.

Using Drosophila melanogaster, we show that the role of protein and carbohydrate on lifespan is indirect, acting by altering the partitioning of limiting amounts of dietary sterols between reproduction and lifespan.

Shorter lifespans in flies fed on high protein: carbohydrate diets can be rescued by supplementing their food with cholesterol. Not only does this fundamentally alter the way we interpret the mechanisms of lifespan extension by dietary restriction, these data highlight the important principle that life histories can be affected by nutrient-dependent trade-offs that are indirect and independent of the nutrients (often macronutrients) that are the focus of study.

This brings us closer to understanding the mechanistic basis of dietary restriction.

Citation

Zanco B, Mirth CK, Sgrò CM, Piper MD (2021) A dietary sterol trade-off determines lifespan responses to dietary restriction in Drosophila melanogaster females. eLife PDF DOI

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