Authors: Belinda van Heerwaarden, Carla M Sgrò, and Vanessa M. Kellermann

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

Abstract

Mounting evidence suggests that ectotherms are already living close to their upper physiological thermal limits. Phenotypic plasticity has been proposed to reduce the impact of climate change in the short-term providing time for adaptation, but the tolerance-plasticity trade-off hypothesis predicts organisms with higher tolerance have lower plasticity. Empirical evidence is mixed, which may be driven by methodological issues such as statistical artefacts, nonlinear reaction norms, threshold shifts or selection.

Here, we examine whether threshold shifts (organisms with higher tolerance require stronger treatments to induce maximum plastic responses) influence tolerance-plasticity trade-offs in hardening capacity for desiccation tolerance and critical thermal maximum (CT_MAX) across Drosophila species with varying distributions/sensitivity to desiccation/heat stress.

We found evidence for threshold shifts in both traits; species with higher heat/desiccation tolerance required longer hardening treatments to induce maximum hardening responses. Species with higher heat tolerance also showed reductions in hardening capacity at higher developmental acclimation temperatures. Trade-off patterns differed depending on the hardening treatment used and the developmental temperature flies were exposed to.

Based on these findings, studies that do not consider threshold shifts, or that estimate plasticity under a narrow set of environments, will have a limited ability to assess trade-off patterns and differences in plasticity across species/populations more broadly.

Citation

Van Heerwaarden B, Sgrò CM, Kellermann VM (2024) Threshold shifts and developmental temperature impact trade-offs between tolerance and plasticity. Proceedings of the Royal Society B: Biological Sciences PDF DOI

Authors: Lesley A Alton, Teresa Kutz, Candice L Bywater, Emily Lombardi, Fiona E Cockerell, Sean Layh, Hugh Winwood-Smith, Pieter A Arnold, Julian E Beaman, Greg M Walter, Keyne Monro, Christen K Mirth, Carla M Sgrò, and Craig R White

Published in: Philosophical Transactions of the Royal Society B: Biological Sciences

Abstract

Metabolic cold adaptation, or Krogh’s rule, is the controversial hypothesis that predicts a monotonically negative relationship between metabolic rate and environmental temperature for ectotherms living along thermal clines measured at a common temperature.

Macrophysiological patterns consistent with Krogh’s rule are not always evident in nature, and experimentally evolved responses to temperature have failed to replicate such patterns. Hence, temperature may not be the sole driver of observed variation in metabolic rate.

We tested the hypothesis that temperature, as a driver of energy demand, interacts with nutrition, a driver of energy supply, to shape the evolution of metabolic rate to produce a pattern resembling Krogh’s rule. To do this, we evolved replicate lines of Drosophila melanogaster at 18, 25 or 28°C on control, low-calorie or low-protein diets.

Contrary to our prediction, we observed no effect of nutrition, alone or interacting with temperature, on adult female and male metabolic rates. Moreover, support for Krogh’s rule was only in females at lower temperatures.

We, therefore, hypothesize that observed variation in metabolic rate along environmental clines arises from the metabolic consequences of environment-specific life-history optimization, rather than because of the direct effect of temperature on metabolic rate.

Citation

Alton LA, Kutz T, Bywater CL, Lombardi E, Cockerell FE, Layh S, Winwood-Smith H, Arnold PA, Beaman JE, Walter GM, Monro K, Mirth CK, Sgrò CM, White CR (2024) Temperature and nutrition do not interact to shape the evolution of metabolic rate. Philosophical Transactions of the Royal Society B: Biological Sciences PDF DOI

Authors: Ashvitha Kannan, Robert J Dugand, Nicholas C Appleton, Stephen F Chenoweth, Carla M Sgrò, and Katrina McGuigan

Published in: Evolution

Abstract

Standing genetic variation, and capacity to adapt to environment change, will ultimately depend on the fitness effects of mutations across the range of environments experienced by contemporary, panmictic, populations.

We investigated how mild perturbations in diet and temperature affect mutational (co)variances of traits that evolve under climatic adaptation, and contribute to individual fitness in Drosophila serrata. We assessed egg-to-adult viability, development time and wing size of 64 lines that had diverged from one another via spontaneous mutation over 30 generations of brother-sister mating.

Our results suggested most mutations have directionally concordant (i.e., synergistic) effects in all environments and both sexes. However, elevated mutational variance under reduced macronutrient conditions suggested environment-dependent variation in mutational effect sizes for development time. We also observed evidence for antagonistic effects under standard versus reduced macronutrient conditions, where these effects were further contingent on temperature (for development time) or sex (for size). Diet also influenced the magnitude and sign of mutational correlations between traits, although this result was largely due to a single genotype (line), which may reflect a rare, large effect mutation.

Overall, our results suggest environmental heterogeneity and environment-dependency of mutational effects could contribute to the maintenance of genetic variance.

Citation

Kannan A, Dugand RJ, Appleton NC, Chenoweth SF, Sgrò CM, McGuigan K (2023) Environmental dependence of mutational (co)variances of adaptive traits. Evolution PDF DOI

Authors: Ary A Hoffmann, Carla M Sgrò, and Belinda van Heerwaarden

Published in: Journal of Experimental Biology

Abstract

A (quite) large set of experiments has been undertaken to assess the potential for evolutionary changes in invertebrates under current and future climate change conditions. These experimental studies have established some key principles that could affect climate change adaptation, yet there remain substantial obstacles in reaching a meaningful predictive framework.

This Review starts with exploring some of the traits considered in individuals and approaches used in assessing evolutionary adaptation relevant to climate, and some of the core findings and their substantial limitations, with a focus on Drosophila. We interpret results in terms of adaptive limits based on population processes versus fundamental mechanistic limits of organisms. We then consider the challenges in moving towards a predictive framework and implications of the findings obtained to date, while also emphasizing the current limited context and the need to broaden it if links to changes in natural populations are to be realized.

Citation

Hoffmann AA, Sgrò CM, Van Heerwaarden B (2023) Testing evolutionary adaptation potential under climate change in invertebrates (mostly Drosophila ): findings, limitations and directions. Journal of Experimental Biology PDF DOI

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

Published in: Functional Ecology

Abstract

1. Understanding the fitness consequences of thermal history is necessary to predict organismal responses to global warming. This is especially challenging for ectotherms with complex life cycles, where distinct life stages can differ in thermal sensitivity, acclimate to different thermal environments and accrue responses to acclimation within and between generations.
2. Although acclimation is often hypothesized to benefit organisms by helping them (or their offspring) to compensate for negative impacts of environmental change, mixed support for this hypothesis highlights the need to assess alternatives. Assessments that explicitly dissect responses across life stages and generations, however, remain limited.
3. We assess alternative hypotheses of acclimation (none, beneficial, colder-is-better and warmer-is-better) within and between generations of a marine tubeworm whose vulnerability to warming rests on survival at early planktonic stages (gametes, embryos and larvae). First, we acclimate parents, gametes and embryos to ambient and projected warmer temperatures (17°C and 22°C) factorially by life stage. Next, we rear offspring with differing acclimation histories to the end of larval development at test temperatures from 10°C to 28°C (lower and upper survival limits respectively). Last, we estimate thermal survival curves for development, and compare them among thermal histories.
4. We show that survival curves are most responsive to parental acclimation followed by acclimation at embryogenesis, but are buffered against acclimation at fertilization. Moreover, curves respond independently to acclimation within and between generations, and respond largely as predicted by the warmer-is-better hypothesis, despite the semblance of beneficial acclimation after successive doses of warmer temperature.
5. Our study demonstrates the varied nature of thermal acclimation and the importance of considering how responses aggregate across complex life cycles when predicting vulnerability to warming.

Citation

Rebolledo AP, Sgrò CM, Monro K (2023) When is warmer better? Disentangling within‐ and between‐generation effects of thermal history on early survival. Functional Ecology PDF DOI

Authors: Fhallon Ware-Gilmore, Mario Novelo, Carla M Sgrò, Matthew D Hall, and Elizabeth A McGraw

Published in: Philosophical Transactions of the Royal Society B

Abstract

The geographical range of the mosquito vector for many human disease-causing viruses, Aedes aegypti, is expanding, in part owing to changing climate. The capacity of this species to adapt to thermal stress will affect its future distributions.

It is unclear how much heritable genetic variation may affect the upper thermal limits of mosquito populations over the long term. Nor are the genetic pathways that confer thermal tolerance fully understood.

In the short term, cells induce a plastic, protective response known as ‘heat shock’.

Using a physiological ‘knockdown’ assay, we investigated mosquito thermal tolerance to characterize the genetic architecture of the trait.

To test variation in mosquito thermal sensitivity, we submerged glass vials containing mosquitoes in a tank of water heated to 42°C, representing the upper critical thermal limit for the mosquitoes as determined by pilot assay. We then monitored the time it took for mosquitoes to become immobilized, or the ‘knockdown’ time, using a barcode scanner. For the other half of this design, we heat-shocked mosquitoes from the same families as the aforementioned mosquitoes measured for knockdown for 15 minutes at 42°C to induce stress-based expression. We then examined the expression of key heat shock genes (Hsps) in selected families.

While families representing the extreme ends of the distribution for knockdown time differed from one another, the trait exhibited low but non-zero broad-sense heritability.

We then explored whether families representing thermal performance extremes differed in their heat shock response by measuring gene expression of heat shock protein-encoding genes Hsp26, Hsp83 and Hsp70.

Contrary to prediction, the families with higher thermal tolerance demonstrated less Hsp expression.

This pattern may indicate that other mechanisms of heat tolerance, rather than heat shock, may underpin the stress response, and the costly production of HSPs may instead signal poor adaptation.

Citation

Ware-Gilmore F, Novelo M, Sgrò CM, Hall MD, McGraw EA (2023) Assessing the role of family level variation and heat shock gene expression in the thermal stress response of the mosquito Aedes aegypti. Philosophical Transactions of the Royal Society B PDF DOI

Authors: Laura M Thompson, Lindsey L Thurman, Carly N Cook, Erik A Beever, Carla M Sgrò, Andrew Battles, Carlos A Botero, John E Gross, Kimberly R Hall, Andrew P Hendry, Ary A Hoffmann, Christopher Hoving, Olivia E LeDee, Claudia Mengelt, Adrienne B Nicotra, Robyn A Niver, Felipe Pérez‐Jvostov, Rebecca M Quiñones, Gregor W Schuurman, Michael K Schwartz, Jennifer Szymanski, and Andrew Whiteley

Published in: Conservation Science and Practice

Abstract

Resource managers have rarely accounted for evolutionary dynamics in the design or implementation of climate change adaptation strategies.

We brought the research and management communities together to identify challenges and opportunities for applying evidence from evolutionary science to support on-the-ground actions intended to enhance species’ evolutionary potential. We amalgamated input from natural-resource practitioners and interdisciplinary scientists to identify information needs, current knowledge that can fill those needs, and future avenues for research.

Three focal areas that can guide engagement include:

1. recognizing when to act,
2. understanding the feasibility of assessing evolutionary potential, and
3. identifying best management practices.

Although researchers commonly propose using molecular methods to estimate genetic diversity and gene flow as key indicators of evolutionary potential, we offer guidance on several additional attributes (and their proxies) that may also guide decision-making, particularly in the absence of genetic data.

Finally, we outline existing decision-making frameworks that can help managers compare alternative strategies for supporting evolutionary potential, with the goal of increasing the effective use of evolutionary information, particularly for species of conservation concern. We caution, however, that arguing over nuance can generate confusion; instead, dedicating increased focus on a decision-relevant evidence base may better lend itself to climate adaptation actions.

Historically, the rusty-patched bumble bee (Bombus affinis) was broadly distributed across prairies and grass-land habitats in eastern and upper-midwest Canada and the USA. The species experienced a widespread and steep decline in the early 2000s, precipitating its endangered status. Today, the species is extant in 11 US states and 1 Canadian province, a >50% reduction in its native range. The exact cause of the decline is unknown, but evidence suggests a synergistic interaction between an introduced pathogen and exposure to pesticides.Image credit: USFWS Midwest Region from United States, via Wikimedia Commons

Citation

Thompson LM, Thurman LL, Cook CN, Beever EA, Sgrò CM, Battles A, Botero CA, Gross JE, Hall KR, Hendry AP, Hoffmann AA, Hoving C, LeDee OE, Mengelt C, Nicotra AB, Niver RA, Pérez‐Jvostov F, Quiñones RM, Schuurman GW, Schwartz MK, Szymanski J, Whiteley A (2023) Connecting research and practice to enhance the evolutionary potential of species under climate change. Conservation Science and Practice PDF DOI

Authors: Brooke Zanco, Lisa Rapley, Joshua N Johnstone, Amy Dedman, Christen K Mirth, Carla M Sgrò, and Matthew DW Piper

Published in: Journal of Insect Physiology

Abstract

Limiting calories or specific nutrients without malnutrition, otherwise known as dietary restriction (DR), has been shown to extend lifespan and reduce reproduction across a broad range of taxa.

Our recent findings in Drosophila melanogaster show that supplementing flies on macronutrient-rich diets with additional cholesterol can extend lifespan to the same extent as DR, while also sustaining high egg production. Thus, DR may be beneficial for lifespan because it reduces egg production which in turn reduces the mother’s demand for sterols, thus supporting longer lifespan. It is also possible that mothers live longer and lay more eggs on high sterol diets because the diet triggers enhanced somatic maintenance and promotes egg production, but at the cost of diminished egg quality.

To test this, we measured the viability of eggs and development of offspring from mothers fed either cholesterol-sufficient or cholesterol-limiting diets.

We found that even when the mother’s diet was completely devoid of cholesterol, viable egg production persisted for ∼10 days. Furthermore, we show that sterol-supplemented flies with long lives lay eggs that have high viability and the same developmental potential as those laid by shorter lived mothers on sterol limiting diets.

These findings suggest that offspring viability is not a hidden cost of lifespan extension seen in response to dietary sterol supplementation.

Sterol-supplemented flies with long lives lay eggs that have high viability and the same developmental potential as those laid by shorter lived mothers on sterol limiting diets.

Citation

Zanco B, Rapley L, Johnstone JN, Dedman A, Mirth CK, Sgrò CM, Piper MDW (2023) Drosophila melanogaster females prioritise dietary sterols for producing viable eggs. Journal of Insect Physiology PDF DOI

Authors: Avishikta Chakraborty, Greg M Walter, Keyne Monro, André N Alves, Christen K Mirth, and Carla M Sgrò

Published in: Journal of Evolutionary Biology

Abstract

Ongoing climate change has forced animals to face changing thermal and nutritional environments. Animals can adjust to such combinations of stressors via plasticity. Body size is a key trait influencing organismal fitness, and plasticity in this trait in response to nutritional and thermal conditions varies among genetically diverse, locally adapted populations. The standing genetic variation within a population can also influence the extent of body size plasticity.

We generated near-isogenic lines from a newly collected population of Drosophila melanogaster at the mid-point of east coast Australia and assayed body size for all lines in combinations of thermal and nutritional stress.

We found that isogenic lines showed distinct underlying patterns of body size plasticity in response to temperature and nutrition that were often different from the overall population response.

We then tested whether plasticity in development time could explain, and therefore regulate, variation in body size to these combinations of environmental conditions. We selected five genotypes that showed the greatest variation in response to combined thermal and nutritional stress and assessed the correlation between response of developmental time and body size.

While we found significant genetic variation in development time plasticity, it was a poor predictor of body size among genotypes. Our results therefore suggest that multiple developmental pathways could generate genetic variation in body size plasticity.

Our study emphasizes the need to better understand genetic variation in plasticity within a population, which will help determine the potential for populations to adapt to ongoing environmental change.

Citation

Chakraborty A, Walter GM, Monro K, Alves AN, Mirth CK, Sgrò CM (2023) Within‐population variation in body size plasticity in response to combined nutritional and thermal stress is partially independent from variation in development time. Journal of Evolutionary Biology PDF DOI

Authors: Vanessa Kellermann, Johannes Overgaard, Carla M Sgrò, and Ary A Hoffmann

Published in: Journal of Evolutionary Biology

Abstract

Sex-based differences in physiological traits may be influenced by both evolutionary and environmental factors.

Here we used male and female flies from >80 Drosophila species reared under common conditions to examine variance in a number of physiological traits including size, starvation, desiccation and thermal tolerance.

Sex-based differences for desiccation and starvation resistance were comparable in magnitude to those for size, with females tending to be relatively more resistant than males. In contrast thermal resistance showed low divergence between the sexes.

Phylogenetic signal was detected for measures of divergence between the sexes, such that species from the Sophophora clade showed larger differences between the sexes than species from the Drosophila clade.

We also found that sex-based differences in desiccation resistance, body size and starvation resistance were weakly associated with climate (annual mean temperature/precipitation seasonality) but the direction and association with environment depended on phylogenetic position.

The results suggest that divergence between the sexes can be linked to environmental factors, while an association with phylogeny suggests sex-based differences persist over long evolutionary time-frames.

Phylogenetic analysis of sex-based differences in desiccation resistance, starvation resistance and body size. Top: Phylogenetic hypothesis of the Drosophila species examined and their sub-groups. Bottom: Sex-based differences mapped onto the phylogeny via ancestral trait reconstruction for continuous characters for traits desiccation resistance (left), body size (middle) and starvation resistance (right). Bars represent the average sexual dimorphism index for each trait, with dots above the bars indicating a significant difference between the sexes when analysed with a one-way ANOVA.

Citation

Kellermann V, Overgaard J, Sgrò CM, Hoffmann AA (2022) Phylogenetic and environmental patterns of sex differentiation in physiological traits across Drosophila species. Journal of Evolutionary Biology PDF DOI