Lab-meeting on Drosophila evolution: epistatic networks and thermal adaptation

Posted by Erik Svensson

There is now a lot of activity in the Drosophila-lab, with one undergraduate student, one postdoc (Natsu) and yesterday also a PRAO-student (my daughter My). Given this, Jessica and I felt it was time to have a lab-meeting focussed on some interesting new research in evolutionary biology, focussed on the Drosophila-system.

We have therefore picked two recent PNAS-papers for discussion, one more genetic and molecular (dealing with epistasis and gene regulatory networks of starvation resistance and chill coma recovery) and one more macroevolutionary, dealing with the evolution of upper thermal limits in a phylogenetic context. Both have in common a focus on thermal adaptation. You will find Abstracts here and here, and Abstracts and titles below.

In addition, we hope Natsu could bring anbd show some printout pictures of the beatiful Wing Interference Patterns (WIP:s) of Drosophila melanogaster inbred lines. This will just be a taster, however, as Natsu will give a more formal seminar later in November telling the lab-group about the ongoing work and some preliminary results.

Time: Tuesday October 23 at 10.30
Place: "Argumentet", 2nd floor

Epistasis dominates the genetic architecture of Drosophila quantitative traits              

Abstract

Epistasis—nonlinear genetic interactions between polymorphic loci—is the genetic basis of canalization and speciation, and epistatic interactions can be used to infer genetic networks affecting quantitative traits. However, the role that epistasis plays in the genetic architecture of quantitative traits is controversial. Here, we compared the genetic architecture of three Drosophila life history traits in the sequenced inbred lines of the Drosophila melanogaster Genetic Reference Panel (DGRP) and a large outbred, advanced intercross population derived from 40 DGRP lines (Flyland). We assessed allele frequency changes between pools of individuals at the extremes of the distribution for each trait in the Flyland population by deep DNA sequencing. The genetic architecture of all traits was highly polygenic in both analyses. Surprisingly, none of the SNPs associated with the traits in Flyland replicated in the DGRP and vice versa. However, the majority of these SNPs participated in at least one epistatic interaction in the DGRP. Despite apparent additive effects at largely distinct loci in the two populations, the epistatic interactions perturbed common, biologically plausible, and highly connected genetic networks. Our analysis underscores the importance of epistasis as a principal factor that determines variation for quantitative traits and provides a means to uncover genetic networks affecting these traits. Knowledge of epistatic networks will contribute to our understanding of the genetic basis of evolutionarily and clinically important traits and enhance predictive ability at an individualized level in medicine and agriculture.

Upper thermal limits of Drosophila are linked to species distributions and strongly constrained phylogenetically

Abstract

Upper thermal limits vary less than lower limits among related species of terrestrial ectotherms. This pattern may reflect weak or uniform selection on upper limits, or alternatively tight evolutionary constraints. We investigated this issue in 94 Drosophila species from diverse climates and reared in a common environment to control for plastic effects that may confound species comparisons. We found substantial variation in upper thermal limits among species, negatively correlated with annual precipitation at the central point of their distribution and also with the interaction between precipitation and maximum temperature, showing that heat resistance is an important determinant of Drosophila species distributions. Species from hot and relatively dry regions had higher resistance, whereas resistance was uncorrelated with temperature in wetter regions. Using a suite of analyses we showed that phylogenetic signal in heat resistance reflects phylogenetic inertia rather than common selection pressures. Current species distributions are therefore more likely to reflect environmental sorting of lineages rather than local adaptation. Similar to previous studies, thermal safety margins were small at low latitudes, with safety margins smallest for species occupying both humid and dry tropical environments. Thus, species from a range of environments are likely to be at risk owing to climate change. Together these findings suggest that this group of insects is unlikely to buffer global change effects through marked evolutionary changes, highlighting the importance of facilitating range shifts for maintaining biodiversity.

 

 

Report from Uppsala: competition, ecological and non-ecological speciation

 Every now and then, one has to visit your enemy and competitor, as Richard Nixon realized in the early 1970'ties, when he visited The People's Republic of China, and shaked hand with communist leader Chairman Mao Zedong (see above). I imagine Nixon felt a bit unsecure when he, as an american, visited a traditional enemy on his home ground, almost like sticking your head in to the lion's den.

Uppsala and Lund Universities, being the oldest and most prestigious universities in Sweden, are often seen as competitors, but luckily we have not been close to armed conflict, like the US and China, and we are hopefully a bit closer to each other than Nixon and Mao. I was therefore honoured when I was offered to sit the thesis committé of Niclas Vallin, one of my colleage Anna Qvarnströms PhD-students, together with Prof. Andrew Hendry from McGill University (Canada). You probably remember that Andrew was also the opponent of my student Fabrice Eroukhmanoff in Lund, a couple of years ago, and then Anna Qvarnström was in the thesis-committe.

The current thesis by Vallin dealt with interspecific competition between flycatcher species on the island of Öland, and was a classical experimental field study which (almost refreshingly!) did not have a single chapter on molecular genetics, which is quite rare these days. Andrew writes a more thorough report about the thesis and its content on his research group blog "Eco-Evo-Evo-Eco".

On Thursday last week, Andrew and I also gave tandem talks at the Evolutionary Biology Centre (EBC) about the importance of ecological speciation, and its alternatives. We both took a critical look at ecological speciation, albeit from different angles, and Andrew writes more about it here.Briefly, Andrew questioned how often ecologically divergent selection leads to the completion of speciation, something which he calls "ecological non-speciation" , whereas I attacked ecological speciation with some examples of radiations which are unlikely to have speciated through ecological means and niche-based divergent selection, which we can call "non-ecological speciation".  

After long and scientific discussions over beers, wine and "Bäversnaps", Andrew and I agreed that we almost understood nothing, and that more research is clearly needed. I therefore would like to take the opportunity to, once again, advertise the ESF-workshop next year on non-adaptive and non-ecological speciation that will take place in Lund next year, on August 18 2012.

Lastly, I have to say I really enjoyed going to Uppsala (in spite of our historical antagonisms!), and to participate both in the thesis-committe of Niklas Vallin, and listen also to the thesis-defence of another PhD-student, Paolo Innocenti, who has worked on the transcriptomic consequences of sexual conflict in Drosophila. Interestingly, Paolo has worked both with Jessica Abbott and Tom Gosden, my two first PhD-students, so this is really a small world. And although Lund might still be the best university in Sweden, there is clearly room also for Uppsala, especially when they open up and collaborate with people from Lund.

Lab-meeting on November 25: signalling sexual and species identity

On Wednesday (November 25), I was thinking that we should do two things during our weekly lab-meeting:

1. We will start by discussing the Nature-paper by Billeter et al. of how Drosophila males and females signal sex and species identity using pheromones ("CHC:s").

Tom Gosden wrote about this paper in an earlier bloggpost, and it seems quite exciting also to those of us who are not particularly interested in pheromone communication. Signalling sex and species identity is clearly a general problem of interest to many evolutionary biologists, and not only those working with Drosophila. The paper can be downloaded here.

2. We will also give Anna Runemark som input on her "half-time seminar" that will take place next week at the Animal Ecology department meeting. Anna brings her laptop and some idéas of her presentation, and the rest of us provide feedback to help her.

Same time and place as usual: "Darwin"-room at 10.00, Wednesday November 25. Any fika-volunteer?

Jessica Abbott: Summary of Research at Queen's

Erik asked me to post an update on the research I've been pursuing since joining the Chippindale lab in 2007. Since I've been in Kingston I've been conducting work on intralocus sexual conflict in Drosophila melanogaster. For those who aren't familiar with intralocus sexual conflict, it is related to the fact that males and females often have different reproductive interests, and therefore different phenotypic optima for a variety of traits. If antagonistic selection pressures are combined with positive intersexual genetic correlations for these traits, one or both sexes may be significantly displaced from their optimum. This displacement is known as intralocus sexual conflict, and has now been demonstrated in both natural and laboratory populations from a wide variety of taxa.

The Chippindale lab has used a powerful method for investigating intralocus sexual conflict: male-limited (ML) evolution in Drosophila melanogaster. When expression of specific haploid genomes was limited to males for over 80 generations, this resulted in an increase in fitness in ML males, and a parallel decrease in fitness in ML females. The phenotypic basis for these fitness differences has been shown to be linked to a displacement of both sexes closer to the male optimum in developmental time, body size, and reproductive behaviour. In addition, it has been demonstrated that intralocus sexual conflict can actually cancel out fitness benefits of sexual selection. When high quality females were mated to high quality males (as would be expected from female choice), this resulted in the production of low-quality offspring, due to the effects of intralocus sexual conflict.

After arriving at Queen's I started an investigation of patterns of phenotypic masculinization in ML flies. I also looked for evidence of increased developmental stability in experimental populations. Using geometric morphometric analysis of wing morphology, I found evidence of masculinization of wing size and wing shape in ML flies of both sexes. I also found increased developmental stability in ML males, which seems to have resulted in decreased developmental stability in ML females. This nicely parallels the results for fitness, where ML males had increased fitness and ML females had decreased fitness (relative to controls).

Because the ML lines had been maintained for over 80 generations when I arrived in 2007 there were concerns about their continued viability, and they were terminated shortly after I started working at Queen's. Once my analysis of wing morphology was finished I therefore decided to start a new male-limited evolution experiment of my own, this time focussing on the X-chromosome. This MLX experiment will also allow me to look at imprinting effects on fitness due to the nature of the experimental evolution protocol.

The protocol for ML X-chromosome evolution is as follows:
Males are mated to females with a double X-chromosome. These DX females (DX = double X) have two X-chromosomes connected at the centromere. They also possess a Y chromosome, so when DX females are mated to normal males, they produce sons that have inherited the Y chromosome from their mothers and the X-chromosome from their fathers. Triple-X and double-Y individuals are not viable. See figure (paternal sex chromosomes are shown in blue, maternal in red, and autosomes in grey).

This father-son transmission of the X-chromosome means that individual X-chromosomes are never expressed in females as long as males are mated to DX females generation after generation. Crucially, this results in male-limited evolution of the X-chromosome. In order to avoid clonal evolution approximately 4-10% recombination between X-chromosomes is allowed using a “recombination box” protocol (see Prasad et al., 2007 for details). This experiment is simultaneously being carried out for two different source populations (LH and Ives) which have completely different histories and culturing protocols. Within each source population I have three replicate populations of selected and control flies, with effective population sizes of 480 individuals for the LH populations and approximately 1500 individuals for the Ives populations. X-chromosomes are usually transmitted from father to daughter, so the father-son transmission generated by this experimental design means that it can be extended to investigate the importance of genomic imprinting to intralocus sexual conflict.

I expect to find similar results to the previous ML experiment (i.e. an increase in male fitness and decrease in female fitness) since the X-chromosome is predicted to be particularly rich in sexually antagonistic loci. I also expect to find a decrease in male fitness due to father-transmission of the X-chromosome. Since X's are usually transmitted father to daughter, you can expect that males might imprint their X chromosomes to benefit female fitness. A male with an X primed to be in a female may therefore have reduced fitness, and some preliminary evidence collected by Stéphanie Bedhomme (a former postdoc in the Chippindale lab) is consistent with this. Perhaps the most interesting aspect of this study is that the MLX evolution protocol will potentially allow short-term evolution of the genomic imprint to adapt to father-son transmission. This is something I will also investigate. I'm currently in the middle of a preliminary fitness assay to investigate imprinting effects. I'm also planning a collaboration with Ted Morrow in Uppsala to look at differences in gene expression due to MLX evolution. I can post more about this later on.

So that's it for now. I'm also planning on running a reciprocal female-limited X-chromosome evolution experiment later on if possible, but I can write more about that later in that case.