Genomic changes associated with adaptation to arid environments in cactophilic Drosophila species

Authors: Rahul V Rane, Stephen L Pearce, Fang Li, Chris Coppin, Michele Schiffer, Jennifer Shirriffs, Carla M Sgrò, Philippa C Griffin, Goujie Zhang, Siu F Lee, Ary A Hoffmann, and John G Oakeshott

Published in: BMC Genomics

Abstract

Insights into the genetic capacities of species to adapt to future climate change can be gained by using comparative genomic and transcriptomic data to reconstruct the genetic changes associated with such adaptations in the past.

Here we investigate the genetic changes associated with adaptation to arid environments, specifically climatic extremes and new cactus hosts, through such an analysis of five repleta group Drosophila species.

We find disproportionately high rates of gene gains in internal branches in the species’ phylogeny where cactus use and subsequently cactus specialisation and high heat and desiccation tolerance evolved. The terminal branch leading to the most heat and desiccation resistant species, Drosophila aldrichi, also shows disproportionately high rates of both gene gains and positive selection. Several Gene Ontology terms related to metabolism were enriched in gene gain events in lineages where cactus use was evolving, while some regulatory and developmental genes were strongly selected in the Drosophila aldrichi branch. Transcriptomic analysis of flies subjected to sublethal heat shocks showed many more downregulation responses to the stress in a heat sensitive versus heat resistant species, confirming the existence of widespread regulatory as well as structural changes in the species’ differing adaptations. Gene Ontology terms related to metabolism were enriched in the differentially expressed genes in the resistant species while terms related to stress response were over-represented in the sensitive one.

Adaptations to new cactus hosts and hot desiccating environments were associated with periods of accelerated evolutionary change in diverse biochemistries. The hundreds of genes involved suggest adaptations of this sort would be difficult to achieve in the timeframes projected for anthropogenic climate change.

Citation

Rane RV, Pearce SL, Li F, Coppin C, Schiffer M, Shirriffs J, Sgrò CM, Griffin PC, Zhang G, Lee SF, Hoffmann AA, Oakeshott JG (2019) Genomic changes associated with adaptation to arid environments in cactophilic Drosophila species, BMC Genomics. PDF DOI

Quantifying the relative contributions of the X chromosome, autosomes, and mitochondrial genome to local adaptation

Authors: Clementine Lasne, Belinda van Heerwaarden, Carla M Sgrò, and Tim Connallon

Published in: Evolution

Abstract

During local adaptation with gene flow, some regions of the genome are inherently more responsive to selection than others.

Recent theory predicts that X‐linked genes should disproportionately contribute to local adaptation relative to other genomic regions, yet this prediction remains to be tested.

We carried out a multigeneration crossing scheme, using two cline‐end populations of Drosophila melanogaster, to estimate the relative contributions of the X chromosome, autosomes, and mitochondrial genome to divergence in four traits involved in local adaptation (wing size, resistance to heat, desiccation, and starvation stresses).

We found that the mitochondrial genome and autosomes contributed significantly to clinal divergence in three of the four traits. In contrast, the X made no significant contribution to divergence in these traits.

Given the small size of the mitochondrial genome, our results indicate that it plays a surprisingly large role in clinal adaptation. In contrast, the X, which represents roughly 20% of the Drosophila genome, contributes negligibly—a pattern that conflicts with theoretical predictions. These patterns reinforce recent work implying a central role of mitochondria in climatic adaptation, and suggest that different genomic regions may play fundamentally different roles in processes of divergence with gene flow.

Citation

Lasne C, Heerwaarden B, Sgrò CM, Connallon T (2019) Quantifying the relative contributions of the X chromosome, autosomes, and mitochondrial genome to local adaptation, Evolution PDF DOI

How does parental environment influence the potential for adaptation to global change?

Authors: Evatt Chirgwin, Dustin J. Marshall, Carla M. Sgrò, and Keyne Monro

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

Abstract

Parental environments are regularly shown to alter the mean fitness of offspring, but their impacts on the genetic variation for fitness, which predicts adaptive capacity and is also measured on offspring, are unclear. Consequently, how parental environments mediate adaptation to environmental stressors, like those accompanying global change, is largely unknown.

Here, using an ecologically important marine tubeworm in a quantitative-genetic breeding design, we tested how parental exposure to projected ocean warming alters the mean survival, and genetic variation for survival, of offspring during their most vulnerable life stage under current and projected temperatures.

Offspring survival was higher when parent and offspring temperatures matched. Across offspring temperatures, parental exposure to warming altered the distribution of additive genetic variance for survival, making it covary across current and projected temperatures in a way that may aid adaptation to future warming. Parental exposure to warming also amplified nonadditive genetic variance for survival, suggesting that compatibilities between parental genomes may grow increasingly important under future warming.

Our study shows that parental environments potentially have broader-ranging effects on adaptive capacity than currently appreciated, not only mitigating the negative impacts of global change but also reshaping the raw fuel for evolutionary responses to it.

Citation

Chirgwin E, Marshall DJ, Sgrò CM, Monro K (2018) How does parental environment influence the potential for adaptation to global change? Proceedings of the Royal Society B: Biological SciencesPDF DOI

In search of a general theory of species’ range evolution

Authors: Tim Connallon and Carla M Sgrò

Published in: PLoS Biology

Abstract

Despite the pervasiveness of the world’s biodiversity, no single species has a truly global distribution. In fact, most species have very restricted distributions. What limits species from expanding beyond their current geographic ranges?

This has been classically treated by ecologists as an ecological problem and by evolutionary biologists as an evolutionary problem. Such a dichotomy is false — the problem of species’ ranges sits firmly within the realm of evolutionary ecology.

In support of this view, Polechová presents new theory that explains species’ range limits with reference to two key factors central to both ecological and evolutionary theory—migration and population size.

This new model sets the scene for empirical tests of range limit theory and builds the case for assisted gene flow as a key management tool for threatened species.

Citation

Connallon T, Sgrò CM (2018) In search of a general theory of species’ range evolution, PLoS Biology. PDF DOI

Evidence for lower plasticity in CT-MAX at warmer developmental temperatures

Authors: Vanessa Kellermann and Carla M. Sgrò

Published in: Journal of Evolutionary Biology

Abstract

Understanding the capacity for different species to reduce their susceptibility to climate change via phenotypic plasticity is essential for accurately predicting species extinction risk.

The climatic variability hypothesis suggests that spatial and temporal variation in climatic variables should select for more plastic phenotypes. However, empirical support for this hypothesis is limited.

Here, we examine the capacity for ten Drosophila species to increase their critical thermal maxima (CTMAX) through developmental acclimation and/or adult heat hardening.

Using four fluctuating developmental temperature regimes, ranging from 13 to 33  °C, we find that most species can increase their CTMAX via developmental acclimation and adult hardening, but found no relationship between climatic variables and absolute measures of plasticity. However, when plasticity was dissected across developmental temperatures, a positive association between plasticity and one measure of climatic variability (temperature seasonality) was found when development took place between 26 and 28 °C, whereas a negative relationship was found when development took place between 20 and 23  °C.

In addition, a decline in CTMAX and egg‐to‐adult viability, a proxy for fitness, was observed in tropical species at the warmer developmental temperatures (26–28 °C); this suggests that tropical species may be at even greater risk from climate change than currently predicted. The combined effects of developmental acclimation and adult hardening on CTMAX were small, contributing to a <0.60 °C shift in CTMAX.

Although small shifts in CTMAX may increase population persistence in the shorter term, the degree to which they can contribute to meaningful responses in the long term is unclear.

Citation

Kellermann V, Sgrò CM (2018) Evidence for lower plasticity in CTMAX at warmer developmental temperatures. Journal of Evolutionary BiologyPDF DOI

Cross‐sex genetic correlations and the evolution of sex‐specific local adaptation: Insights from classical trait clines in Drosophila melanogaster

Authors: Clémentine Lasne, Sandra B Hangartner, Tim Connallon, and Carla M. Sgrò

Published in: Evolution

Abstract

Natural selection varies widely among locations of a species’ range, favoring population divergence and adaptation to local environmental conditions. Selection also differs between females and males, favoring the evolution of sexual dimorphism. Both forms of within‐species evolutionary diversification are widely studied, though largely in isolation, and it remains unclear whether environmental variability typically generates similar or distinct patterns of selection on each sex.

Studies of sex‐specific local adaptation are also challenging because they must account for genetic correlations between female and male traits, which may lead to correlated patterns of trait divergence between sexes, whether or not local selection patterns are aligned or differ between the sexes.

We quantified sex‐specific divergence in five clinally variable traits in Drosophila melanogasterthat individually vary in their magnitude of cross‐sex genetic correlation (i.e., from moderate to strongly positive).

In all five traits, we observed parallel male and female clines, regardless of the magnitude of their genetic correlation. These patterns imply that parallel spatial divergence of female and male traits is a reflection of sexually concordant directional selection imposed by local environmental conditions. In such contexts, genetic correlations between the sexes promote, rather than constrain, local adaptation to a spatially variable environment.

Citation

Lasne C, Hangartner SB, Connallon T, Sgrò CM (2018) Cross-sex genetic correlations and the evolution of sex-specific local adaptation: Insights from classical trait clines in Drosophila melanogaster, Evolution PDF DOI

Understanding managers’ and scientists’ perspectives on opportunities to achieve more evolutionarily enlightened management in conservation

Authors: Carly N Cook and Carla M Sgrò

Published in: Evolutionary Applications

Abstract

Despite wide acceptance that conservation could benefit from greater attention to principles and processes from evolutionary biology, little attention has been given to quantifying the degree to which relevant evolutionary concepts are being integrated into management practices. There has also been increasing discussion of the potential reasons for a lack of evolutionarily enlightened management, but no attempts to understand the challenges from the perspective of those making management decisions.

In this study, we asked conservation managers and scientists for their views on the importance of a range of key evolutionary concepts, the degree to which these concepts are being integrated into management, and what would need to change to support better integration into management practices.

We found that while managers recognize the importance of a wide range of evolutionary concepts for conservation outcomes, they acknowledge these concepts are rarely incorporated into management. Managers and scientists were in strong agreement about the range of barriers that need to be overcome, with a lack of knowledge reported as the most important barrier to better integration of evolutionary biology into conservation decision‐making.

Although managers tended to be more focused on the need for more training in evolutionary biology, scientists reported greater engagement between managers and evolutionary biologists as most important to achieve the necessary change. Nevertheless, the challenges appear to be multifaceted, and several are outside the control of managers, suggesting solutions will need to be multidimensional.

Citation

Cook CN, Sgrò CM (2018) Understanding managers’ and scientists’ perspectives on opportunities to achieve more evolutionarily enlightened management in conservation, Evolutionary Applications. PDF DOI