Plasticity for desiccation tolerance across Drosophila species is affected by phylogeny and climate in complex ways

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

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

Abstract

Comparative analyses of ectotherm susceptibility to climate change often focus on thermal extremes, yet responses to aridity may be equally important.

Here we focus on plasticity in desiccation resistance, a key trait shaping distributions of Drosophila species and other small ectotherms.

We examined the extent to which 32 Drosophila species, varying in their distribution, could increase their desiccation resistance via phenotypic plasticity involving hardening, linking these responses to environment, phylogeny and basal resistance.

We found no evidence to support the seasonality hypothesis; species with higher hardening plasticity did not occupy environments with higher and more seasonal precipitation. As basal resistance increased, the capacity of species to respond via phenotypic plasticity decreased, suggesting plastic responses involving hardening may be constrained by basal resistance. Trade-offs between basal desiccation resistance and plasticity were not universal across the phylogeny and tended to occur within specific clades. Phylogeny, environment and trade-offs all helped to explain variation in plasticity for desiccation resistance but in complex ways.

These findings suggest some species have the ability to counter dry periods through plastic responses, whereas others do not; and this ability will depend to some extent on a species’ placement within a phylogeny, along with its basal level of resistance.

Citation

Kellermann V, Hoffmann AA, Overgaard J, Loeschcke V, Sgrò CM (2018) Plasticity for desiccation tolerance across Drosophila species is affected by phylogeny and climate in complex ways. Proceedings of the Royal Society B: Biological Sciences. PDF DOI

Artificial barriers prevent genetic recovery of small isolated populations of a low-mobility freshwater fish

Authors: Rhys A Coleman, Bertrand Gauffre, Anna Pavlova, Luciano  B Beheregaray, Joanne Kearns, Jarod Lyon, Minami Sasaki, Raphael Leblois, Carla M Sgrò, and Paul Sunnucks

Published in: Heredity

Abstract

Habitat loss and fragmentation often result in small, isolated populations vulnerable to environmental disturbance and loss of genetic diversity. Low genetic diversity can increase extinction risk of small populations by elevating inbreeding and inbreeding depression, and reducing adaptive potential. Due to their linear nature and extensive use by humans, freshwater ecosystems are especially vulnerable to habitat loss and fragmentation.

Although the effects of fragmentation on genetic structure have been extensively studied in migratory fishes, they are less understood in low-mobility species.

We estimated impacts of instream barriers on genetic structure and diversity of the low-mobility river blackfish (Gadopsis marmoratus) within five streams separated by weirs or dams constructed 45–120 years ago.

We found evidence of small-scale (<13 km) genetic structure within reaches unimpeded by barriers, as expected for a fish with low mobility. Genetic diversity was lower above barriers in small streams only, regardless of barrier age. In particular, one isolated population showed evidence of a recent bottleneck and inbreeding. Differentiation above and below the barrier (FST = 0.13) was greatest in this stream, but in other streams did not differ from background levels.

Spatially explicit simulations suggest that short-term barrier effects would not be detected with our data set unless effective population sizes were very small (<100).

Our study highlights that, in structured populations, the ability to detect short-term genetic effects from barriers is reduced and requires more genetic markers compared to panmictic populations. We also demonstrate the importance of accounting for natural population genetic structure in fragmentation studies.

Citation

Coleman RA, Gauffre B, Pavlova A, Beheregaray LB, Kearns J, Lyon J, Sasaki M, Leblois R, Sgro C, Sunnucks P (2018) Artificial barriers prevent genetic recovery of small isolated populations of a low-mobility freshwater fish. Heredity PDF DOI

Basal resistance enhances warming tolerance of alien over indigenous species across latitude

Authors: Charlene Janion-Scheepers, Laura Phillips, Carla M Sgrò, Grant A Duffy, Rebecca Hallas, and Steven L Chown

Published in: Proceedings of the National Academy of Sciences of the United States of America, volume 115, issue 1

Abstract

Soil systems are being increasingly exposed to the interactive effects of biological invasions and climate change, with rising temperatures expected to benefit alien over indigenous species.

We assessed this expectation for an important soil-dwelling group, the springtails, by determining whether alien species show broader thermal tolerance limits and greater tolerance to climate warming than their indigenous counterparts.

We found that, from the tropics to the sub-Antarctic, alien species have the broadest thermal tolerances and greatest tolerance to environmental warming. Both groups of species show little phenotypic plasticity or potential for evolutionary change in tolerance to high temperature.

These trait differences between alien and indigenous species suggest that biological invasions will exacerbate the impacts of climate change on soil systems, with profound implications for terrestrial ecosystem functioning.

Citation

Janion-Scheepers C, Phillips L, Sgrò CM, Duffy GA, Hallas R, Chown SL (2018) Basal resistance enhances warming tolerance of alien over indigenous species across latitude. Proceedings of the National Academy of Sciences of the United States of America PDF DOI

Comparative studies of critical physiological limits and vulnerability to environmental extremes in small ectotherms: How much environmental control is needed?

Authors: Ary A Hoffmann and Carla M Sgrò

Published in: Integrative Zoology, volume 13, issue 4 (July 2018)

Abstract

Researchers and practitioners are increasingly using comparative assessments of critical thermal and physiological limits to assess the relative vulnerability of ectothermic species to extreme thermal and aridity conditions occurring under climate change.

In most assessments of vulnerability, critical limits are compared across taxa exposed to different environmental and developmental conditions. However, many aspects of vulnerability should ideally be compared when species are exposed to the same environmental conditions, allowing a partitioning of sources of variation such as used in quantitative genetics.

This is particularly important when assessing the importance of different types of plasticity to critical limits, using phylogenetic analyses to test for evolutionary constraints, isolating genetic variants that contribute to limits, characterizing evolutionary interactions among traits limiting adaptive responses, and when assessing the role of cross generation effects. However, vulnerability assessments based on critical thermal/physiological limits also need to take place within a context that is relevant to field conditions, which is not easily provided under controlled environmental conditions where behavior, microhabitat, stress exposure rates and other factors will differ from field conditions.

There are ways of reconciling these requirements, such as by taking organisms from controlled environments and then testing their performance under field conditions (or vice versa).

While comparisons under controlled environments are challenging for many taxa, assessments of critical thermal limits and vulnerability will always be incomplete unless environmental effects within and across generations are considered, and where the ecological relevance of assays measuring critical limits can be established.

Citation

Hoffmann AA, Sgrò CM (2018) Comparative studies of critical physiological limits and vulnerability to environmental extremes in small ectotherms: How much environmental control is needed? Integrative Zoology PDF DOI

Transcriptional profiles of plasticity for desiccation stress in Drosophila

Authors: Allannah S Clemson, Carla M Sgrò, and Marina Telonis-Scott

Published in: Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology

Abstract

We examined the transcriptional responses of desiccation resistance candidate genes in populations of Drosophila melanogaster divergent for desiccation resistance and in capacity to improve resistance via phenotypic plasticity.

Adult females from temperate and tropical eastern Australian populations were exposed to a rapid desiccation hardening (RDH) treatment, and groups without RDH to acute desiccation stress, and the transcript expression of 12 candidate desiccation genes were temporally profiled during, and in recovery from stress.

We found that desiccation exposure resulted in largely transitory, stress-specific transcriptional changes in all but one gene. However linking the expression profiles to the population-level phenotypic divergence was difficult given subtle, and time-point specific population expression variation. Nonetheless, rapid desiccation hardening had the largest effect on gene expression, resulting in distinct molecular profiles.

We report a hitherto uncharacterised desiccation molecular hardening response where prior exposure essentially ‘primes’ genes to respond to subsequent stress without discernible transcript changes prior to stress. This, taken together with some population gene expression variation of several bona fide desiccation candidates associated with different water balance strategies speaks of the complexity of natural desiccation resistance and plasticity and provides new avenues for understanding the molecular basis of a trait of ecological significance.

Citation

Clemson AS, Sgrò CM, Telonis-Scott M (2018) Transcriptional profiles of plasticity for desiccation stress in Drosophila, Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology PDF DOI

The quantitative genetic basis of clinal divergence in phenotypic plasticity

Authors: Belinda van Heerwaarden and Carla M Sgrò

Published in: Evolution

Abstract

Phenotypic plasticity is thought to be an important mechanism for adapting to environmental heterogeneity. Nonetheless, the genetic basis of plasticity is still not well understood.

In Drosophila melanogaster and D. simulans, body size and thermal stress resistance show clinal patterns along the east coast of Australia, and exhibit plastic responses to different developmental temperatures. The genetic basis of thermal plasticity, and whether the genetic effects underlying clinal variation in traits and their plasticity are similar, remains unknown.

Here, we use line‐cross analyses between a tropical and temperate population of Drosophila melanogaster and D. simulans developed at three constant temperatures (18°C, 25°C, and 29°C) to investigate the quantitative genetic basis of clinal divergence in mean thermal response (elevation) and plasticity (slope and curvature) for thermal stress and body size traits.

Generally, the genetic effects underlying divergence in mean response and plasticity differed, suggesting that different genetic models may be required to understand the evolution of trait means and plasticity.

Furthermore, our results suggest that nonadditive genetic effects, in particular epistasis, may commonly underlie plastic responses, indicating that current models that ignore epistasis may be insufficient to understand and predict evolutionary responses to environmental change.

Citation

van Heerwaarden B, Sgrò CM (2017) The quantitative genetic basis of clinal divergence in phenotypic plasticity, Evolution PDF DOI

Experimental support that natural selection has shaped the latitudinal distribution of mitochondrial haplotypes in in Australian Drosophila melanogaster

Authors: M Florencia Camus, Jonci N Wolff, Carla M Sgrò, and Damian K Dowling

Published in: Molecular Biology and Evolution, volume 34, issue 10 (October 2017)

Abstract

Cellular metabolism is regulated by enzyme complexes within the mitochondrion, the function of which are sensitive to the prevailing temperature. Such thermal sensitivity, coupled with the observation that population frequencies of mitochondrial haplotypes tend to associate with latitude, altitude, or climatic regions across species distributions, led to the hypothesis that thermal selection has played a role in shaping standing variation in the mitochondrial DNA (mtDNA) sequence.

This hypothesis, however, remains controversial, and requires evidence that the distribution of haplotypes observed in nature corresponds with the capacity of these haplotypes to confer differences in thermal tolerance. Specifically, haplotypes predominating in tropical climates are predicted to encode increased tolerance to heat stress, but decreased tolerance to cold stress.

We present direct evidence for these predictions, using mtDNA haplotypes sampled from the Australian distribution of Drosophila melanogaster. We show that the ability of flies to tolerate extreme thermal challenges is affected by sequence variation across mtDNA haplotypes, and that the thermal performance associated with each haplotype corresponds with its latitudinal prevalence.

The haplotype that predominates at low (subtropical) latitudes confers greater resilience to heat stress, but lower resilience to cold stress, than haplotypes predominating at higher (temperate) latitudes.

We explore molecular mechanisms that might underlie these responses, presenting evidence that the effects are in part regulated by SNPs that do not change the protein sequence. Our findings suggest that standing variation in the mitochondrial genome can be shaped by thermal selection, and could therefore contribute to evolutionary adaptation under climatic stress.

Citation

Camus MF, Wolff JN, Sgrò CM, Dowling DK (2017) Experimental support that natural selection has shaped the latitudinal distribution of mitochondrial haplotypes in Australian Drosophila melanogaster, Molecular Biology and Evolution PDF DOI