Evolution Highlight: Contributions of the X chromosome, autosomes, and mitochondrial genome to local adaptation

Each month, the Evolution Highlights series will highlight some of the interesting and varied papers published within the last few years in Evolution. The goal of these Evolution Highlights is to let our readers learn more about how the highlighted study came into existence, and to invite the authors to share stories and tips from the perspective of a recently published author. We welcome nominations and self-nominations for the Evolution Highlights. Find out how to submit a paper here.

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"Quantifying the relative contributions of the X chromosome, autosomes, and mitochondrial genome to local adaptation"
Lasne, C., Van Heerwaarden, B., Sgrò, C.M. and Connallon, T. (2019), Quantifying the relative contributions of the X chromosome, autosomes, and mitochondrial genome to local adaptation*. Evolution, 73: 262-277. https://doi.org/10.1111/evo.13647
https://onlinelibrary.wiley.com/doi/abs/10.1111/evo.13647

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.

Evolution Highlight by Clementine Lasne
Institute of Science and Technology Austria, Institute of Science and Technology Austria

What gave you the idea for this study?

My PhD advisors and I had just developed and published a new theoretical study in which we predicted that—under many different scenarios of gene flow, selection and genetic dominance—local adaptation should be facilitated when the allele(s) under selection are X-linked rather than autosomal.

What was the big question you were trying to ask and why was it exciting?

The big question was whether the X-chromosome did indeed make a larger contribution to local adaptation than the autosomes, as predicted by our new theory. I do not know if there is anything more exciting for a PhD student (or biologist, in general) than the feeling of satisfaction and achievement one gets from empirically testing his/her own theoretical model.

From your perspective, what was the most interesting or intriguing aspect of this study?

The most intriguing aspect of the study was the unexpected results! The X chromosome failed to play a disproportionately large role in the evolution of local adaptation for any of the traits we examined. Instead, the mitochondrial genome became the (unexpected) star of the show. Once the disappointment of not empirically verifying our theoretical predictions had passed, we revisited our theory to include the mitochondrial genome and found that our results made sense. This was the most interesting part of the study.

Were there any unexpected logistical or technical challenges you had to address?

Although not technical per se, the biggest challenge of this study was obtaining a large enough sample size to determine with certainty whether or not there was a large X-effect in local adaptation. While morphological traits such as wing size did not require particularly large sample sizes, the stress resistance traits we used are physiological traits that are typically quite “noisy” and difficult to measure. We therefore did a power analysis, guided by data that I had previously collected from these populations and published, and settled on sample sizes that would give us reasonable power to test our hypotheses.

Did your work take you to any interesting locations? If so, what were they like?

The two populations of Drosophila melanogaster used for this study were in fact part of a large field collection during which a colleague and I drove from Melbourne to Cairns (3000km along the east coast of Australia!), with regular stops to collect populations of Drosophila along the way. This is no secret to Drosophila biologists, but the best places to find large numbers of Drosophila are wineries!

Did you have to learn any new analytical techniques for this study?

Most of the analytical techniques were new to me. But I particularly enjoyed learning to calculate the confidence intervals around the chromosomal contribution indices using simulated random draws, and the line-cross analysis technique used to assess the importance of additive from non-additive effects on the traits we examined.

What was the most challenging part of analyzing your data?

Making peace with the fact we were not finding any large-X effects...

How did writing up this study compare to previous paper writing experiences?

This study was the third and last chapter of my PhD thesis. With the valuable experience of two previous publications, as well as the motivation of testing my theoretical predictions, the writing of this paper was mostly pleasant. It was definitely a lot easier than writing the theory manuscript, which was my first publication ever (and is now the study I am the proudest of).

What was the review / revision process like?

The review process went smoothly. My co-authors and I were pleased by the positive feedback we received from reviewers, and their useful suggestions for how we could improve the paper. Then I remember immediately thinking “don’t get used to this!”.

Do you have any writing tips for others?

More experienced scientists would probably have very valuable tips on books to read to improve your grammar, but here are the things that were most useful to me, as a young and unexperienced writer. Firstly, don’t let your impostor syndrome take over your writing. Start by clearly writing on top of the page the research question and your hypothesis. Then do an outline of each section of the manuscript (bullet points will do). Get feedback on this outline from your supervisors before writing the paragraphs. Finally, do yourself a favor by including references to the literature as you write. There is nothing more frustrating than spending hours searching for the one statement you clearly remember reading a few days ago but cannot remember where!

What do you think will be the lasting impact of this study?

There is still a lot to learn about the genetic basis of adaptation to a changing environment. The approach we proposed in this study could very well be applied to other species exhibiting wide geographic distributions and divergence for ecologically important traits. Our approach could also be used to explore the genetic basis of population divergence in projects involving experimental evolution.


 
 

 
  
 
 
 
 
 
 

 
 
 
 
 
 
 
 

Heat resistance assay set-up
 
 
 
 
 
 

 
 
 
 
 
 
 


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