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

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, John G. Oakeshott

Research output: Contribution to journalArticleResearchpeer-review

Abstract

Background: 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. 

Results: 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. 

Conclusion: 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.

Original languageEnglish
Article number52
Number of pages22
JournalBMC Genomics
Volume20
Issue number1
DOIs
Publication statusPublished - 16 Jan 2019

Keywords

  • Cactophilic Drosophila
  • Comparative genomics
  • Heat stress
  • Host adaptation
  • Transcriptomics

Cite this

Rane, R. V., Pearce, S. L., Li, F., Coppin, C., Schiffer, M., Shirriffs, J., ... Oakeshott, J. G. (2019). Genomic changes associated with adaptation to arid environments in cactophilic Drosophila species. BMC Genomics, 20(1), [52]. https://doi.org/10.1186/s12864-018-5413-3
Rane, Rahul V. ; Pearce, Stephen L. ; Li, Fang ; Coppin, Chris ; Schiffer, Michele ; Shirriffs, Jennifer ; Sgrò, Carla M. ; Griffin, Philippa C. ; Zhang, Goujie ; Lee, Siu F. ; Hoffmann, Ary A. ; Oakeshott, John G. / Genomic changes associated with adaptation to arid environments in cactophilic Drosophila species. In: BMC Genomics. 2019 ; Vol. 20, No. 1.
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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, vol. 20, no. 1, 52. https://doi.org/10.1186/s12864-018-5413-3

Genomic changes associated with adaptation to arid environments in cactophilic Drosophila species. / Rane, Rahul V.; Pearce, Stephen L.; Li, Fang; Coppin, Chris; Schiffer, Michele; Shirriffs, Jennifer; Sgrò, Carla M.; Griffin, Philippa C.; Zhang, Goujie; Lee, Siu F.; Hoffmann, Ary A.; Oakeshott, John G.

In: BMC Genomics, Vol. 20, No. 1, 52, 16.01.2019.

Research output: Contribution to journalArticleResearchpeer-review

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AU - Rane, Rahul V.

AU - Pearce, Stephen L.

AU - Li, Fang

AU - Coppin, Chris

AU - Schiffer, Michele

AU - Shirriffs, Jennifer

AU - Sgrò, Carla M.

AU - Griffin, Philippa C.

AU - Zhang, Goujie

AU - Lee, Siu F.

AU - Hoffmann, Ary A.

AU - Oakeshott, John G.

PY - 2019/1/16

Y1 - 2019/1/16

N2 - Background: 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. Results: 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. Conclusion: 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.

AB - Background: 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. Results: 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. Conclusion: 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.

KW - Cactophilic Drosophila

KW - Comparative genomics

KW - Heat stress

KW - Host adaptation

KW - Transcriptomics

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