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

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