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

Authors: Matthew DW Piper, Brooke Zanco, Carla M Sgrò, Margo I Adler, Christen K Mirth, and Russell Bonduriansky

Published in: The Federation of European Biochemical Societies (FEBS) Journal

Abstract

Reducing overall food intake, or lowering the proportion of protein relative to other macronutrients, can extend the lifespan of diverse organisms. A number of mechanistic theories have been developed to explain this phenomenon, mostly assuming that the molecules connecting diet to lifespan are evolutionarily conserved.

A recent study using Drosophila melanogaster females has pinpointed a single essential micronutrient that can explain how lifespan is changed by dietary restriction. Here, we propose a likely mechanism for this observation, which involves a trade-off between lifespan and reproduction, but in a manner that is conditional on the dietary supply of an essential micronutrient – a sterol.

Importantly, these observations argue against previous evolutionary theories that rely on constitutive resource reallocation or damage directly inflicted by reproduction. Instead, they are compatible with a model in which the inverse relationship between lifespan and food level is caused by the consumer suffering from varying degrees of malnutrition when maintained on lab food.

The data also indicate that animals on different lab foods may suffer from different nutritional imbalances and that the mechanisms by which dietary restriction benefits the lifespan of different species may vary.

This means that translating the mechanistic findings from lab animals to humans will not be simple and should be interpreted in light of the range of challenges that have shaped each organism’s lifespan in the wild and the composition of the natural diets upon which they would feed.

Citation

Piper MDW, Zanco B, Sgrò CM, Adler MI, Mirth CK, Bonduriansky R (2022) Dietary restriction and lifespan: adaptive reallocation or somatic sacrifice? The FEBS Journal PDF DOI

Authors: Sandra Hangartner, Carla M Sgrò, Tim Connallon, and Isobel Booksmythe

Published in: Ecology Letters

Abstract

Populations must adapt to environmental changes to remain viable. Both evolution and phenotypic plasticity contribute to adaptation, with plasticity possibly being more important for coping with rapid change.

Adaptation is complex in species with separate sexes, as the sexes can differ in the strength or direction of natural selection, the genetic basis of trait variation, and phenotypic plasticity. Many species show sex differences in plasticity, yet how these differences influence extinction susceptibility remains unclear.

We first extend theoretical models of population persistence in changing environments and show that persistence is affected by sexual dimorphism for phenotypic plasticity, trait genetic architecture, and sex-specific selection.

Our models predict that female-biased adaptive plasticity — particularly in traits with modest-to-low cross-sex genetic correlations — typically promotes persistence, though we also identify conditions where sexually monomorphic or male-biased plasticity promotes persistence.

We then perform a meta-analysis of sex-specific plasticity under manipulated thermal conditions.

Although examples of sexually dimorphic plasticity are widely observed, systematic sex differences are rare. An exception — cold resistance — is systematically female-biased and represents a trait wherein sexually dimorphic plasticity might elevate population viability in changing environments.

We discuss our results in light of debates about the roles of evolution and plasticity in extinction susceptibility.

Citation

Hangartner S, Sgrò CM, Connallon T, Booksmythe I (2022) Sexual dimorphism in phenotypic plasticity and persistence under environmental change: An extension of theory and meta‐analysis of current data. Ecology Letters PDF DOI

Authors: André N Alves, Carla M Sgrò, Matthew DW Piper, and Christen K Mirth

Published in: Frontiers in Cell and Developmental Biology

Abstract

Nutrition shapes a broad range of life-history traits, ultimately impacting animal fitness. A key fitness-related trait, female fecundity is well known to change as a function of diet. In particular, the availability of dietary protein is one of the main drivers of egg production, and in the absence of essential amino acids egg laying declines. However, it is unclear whether all essential amino acids have the same impact on phenotypes like fecundity.

Using a holidic diet, we fed adult female Drosophila melanogaster diets that contained all necessary nutrients except one of the 10 essential amino acids and assessed the effects on egg production.

For most essential amino acids, depleting a single amino acid induced as rapid a decline in egg production as when there were no amino acids in the diet. However, when either methionine or histidine were excluded from the diet, egg production declined more slowly.

Next, we tested whether general control non-derepressible 2 (GCN2) and Target of Rapamycin (TOR) mediated this difference in response across amino acids.

While mutations in GCN2 did not eliminate the differences in the rates of decline in egg laying among amino acid drop-out diets, we found that inhibiting TOR signalling caused egg laying to decline rapidly for all drop-out diets. TOR signalling does this by regulating the yolk-forming stages of egg chamber development.

Our results suggest that amino acids differ in their ability to induce signalling via the TOR pathway. This is important because if phenotypes differ in sensitivity to individual amino acids, this generates the potential for mismatches between the output of a pathway and the animal’s true nutritional status.

Citation

Alves AN, Sgrò CM, Piper MDW, Mirth CK (2022) Target of rapamycin drives unequal responses to essential amino acid depletion for egg laying in Drosophila melanogaster. Frontiers in Cell and Developmental Biology PDF DOI

Authors: Yvonne Willi, Torsten N Kristensen, Carla M Sgrò, Andrew R Weeks, Michael Ørsted, and Ary A Hoffmann

Published in: Proceedings of the National Academy of Sciences

Abstract

About 50 years ago, Crow and Kimura and Ohta and Kimura laid the foundations of conservation genetics by predicting the relationship between population size and genetic marker diversity. This work sparked an enormous research effort investigating the importance of population dynamics, in particular small population size, for population mean performance, population viability, and evolutionary potential.

In light of a recent perspective that challenges some fundamental assumptions in conservation genetics, it is timely to summarize what the field has achieved, what robust patterns have emerged, and worthwhile future research directions.

We consider theory and methodological breakthroughs that have helped management, and we outline some fundamental and applied challenges for conservation genetics.

Citation

Willi Y, Kristensen TN, Sgrò CM, Weeks AR, Ørsted M, Hoffmann AA (2022) Conservation genetics as a management tool: The five best-supported paradigms to assist the management of threatened species. Proceedings of the National Academy of Sciences PDF DOI

Authors: Fang Li, Rahul V Rane, Victor Luria, Zijun Xiong, Jiawei Chen, Zimai Li, Renee A Catullo, Philippa C Griffin, Michele Schiffer, Stephen Pearce, Siu Fai Lee, Kerensa McElroy, Ann Stocker, Jennifer Shirriffs, Fiona Cockerell, Chris Coppin, Carla M Sgrò, Amir Karger, John W Cain, Jessica A Weber, Gabriel Santpere, Marc W Kirschner, Ary A Hoffmann, John G Oakeshott, and Guojie Zhang

Published in: Molecular Ecology Resources

Abstract

Many Drosophila species differ widely in their distributions and climate niches, making them excellent subjects for evolutionary genomic studies.

Here, we have developed a database of high-quality assemblies for 46 Drosophila species and one closely related Zaprionus. Fifteen of the genomes were newly sequenced, and 20 were improved with additional sequencing. New or improved annotations were generated for all 47 species, assisted by new transcriptomes for 19.

Phylogenomic analyses of these data resolved several previously ambiguous relationships, especially in the melanogaster species group. However, it also revealed significant phylogenetic incongruence among genes, mainly in the form of incomplete lineage sorting in the subgenus Sophophora but also including asymmetric introgression in the subgenus Drosophila.

Using the phylogeny as a framework and taking into account these incongruences, we then screened the data for genome-wide signals of adaptation to different climatic niches.

First, phylostratigraphy revealed relatively high rates of recent novel gene gain in three temperate pseudoobscura and five desert-adapted cactophilic mulleri subgroup species.

Second, we found differing ratios of nonsynonymous to synonymous substitutions in several hundred orthologues between climate generalists and specialists, with trends for significantly higher ratios for those in tropical and lower ratios for those in temperate-continental specialists respectively than those in the climate generalists.

Finally, resequencing natural populations of 13 species revealed tropics-restricted species generally had smaller population sizes, lower genome diversity and more deleterious mutations than the more widespread species.

We conclude that adaptation to different climates in the genus Drosophila has been associated with large-scale and multifaceted genomic changes.

Phylogeny and climate niches of the 47 species. Species with names in bold are newly sequenced, those in black are improved by additional sequences generated in this study and those in grey are as previously published. Stars (★)indicate the species for which we added transcriptome data, diamonds (◆) indicates those for which we resequenced multiple individuals. Pie chart areas for each node show the proportions of the three possible topologies for the corresponding branch, with blue denoting the most common topology (i.e., the species tree, as shown) and red and orange the two alternatives (i.e., with each of the two daughter lineages in the species tree as the outgroup instead). The three nodes indicated with red dots are those for which dates had been estimated by Tamura et al. (2004). Climate zones occupied by each species according to the Köppen classification are presented on the right, with the shaded portions denoting presence in that environment.

Citation

Li F, Rane RV, Luria V, Xiong Z, Chen J, Li Z, Catullo RA, Griffin PC, Schiffer M, Pearce S, Lee SF, McElroy K, Stocker A, Shirriffs J, Cockerell F, Coppin C, Sgrò CM, Karger A, Cain JW, Weber JA, Santpere G, Kirschner MW, Hoffmann AA, Oakeshott JG, Zhang G (2022) Phylogenomic analyses of the genus Drosophila reveals genomic signals of climate adaptation. Molecular Ecology Resources PDF DOI