Lab-meeting: negative frequency-dependent selection and a rock-paper-scissor game going on in Drosophila melanogaster?

Posted by Erik Svensson

Inspired by the recent media buss of our sexual selection study on Drosophila melanogaster, which got nice coverage in major media such as New York Times and Washington Post, I would like to dedicate the next lab-meeting other fascinating aspects of fruit flies and sexual selection. It is amazing that so much still remains to be known about this well-studied animal, isn't it?

This time we will discuss an interesting question: is there evidence of a rock-paper-scissor game in D. melanogaster, and if so does it maintain genetic variation?

The article we will discuss was published in Molecular Ecology, and you can find it here. There is also a nice and a brief commenting article by Adam Chippindale in the same issue, which you can find here.

For those of you who do not know what the rock-paper-scissor game is, it is a special form of negative frequency-dependent selection, where each genotype (or morph) has its own strength and weakness, and all morphs co-exist over evolutionary time, due to a particular fitness pay off structure. The first empirical example of a rock-paper-scissor game that was described was for the colour polymorphic side-blotched lizard (Uta stansburiana) in California, by Barry Sinervo. For years, many have thought this system was unique and perhaps not very representative, but the new fruit fly study might suggest otherwise.

 I hope you will enjoy these articles and the discussion. Abstract is found below. Time and place as usual:

When: Tuesday, November 11, at 10.30
Where: "Argumentet", 2nd floor, Ecology Building.

Welcome!

Natural genetic variation in male reproductive genes contributes to nontransitivity of sperm competitive ability in Drosophila melanogaster

1. Rui Zhang,
2. Andrew G. Clark and
3. Anthony C. Fiumera

Abstract

Female Drosophila melanogaster frequently mate with multiple males, and the success of a given male depends not only on his genotype but also on the genotype of his competitor. Here, we assess how natural genetic variation affects male–male interactions for traits influencing pre- and postcopulatory sexual selection. Males from a set of 66 chromosome substitution lines were competed against each other in a ‘round-robin’ design, and paternity was scored using bulk genotyping. We observed significant effects of the genotype of the first male to mate, the second male to mate and an interaction between the males for measures of male mating rate and sperm utilization. We also identified specific combinations of males who show nontransitive patterns of reproductive success and engage in ‘rock-paper-scissors’ games. We then tested for associations between 245 polymorphisms in 32 candidate male reproductive genes and male reproductive success. We identified eight polymorphisms in six reproductive genes that associate with male reproductive success independent of the competitor (experimentwise P < 0.05). We also identified four SNPs in four different genes where the relative reproductive success of the alternative alleles changes depending on the competing males' genetic background (experimentwise P < 0.05); two of these associations include premature stop codons. This may be the first study that identifies the genes contributing to nontransitivity among males and further highlights that ‘rock-paper-scissors’ games could be an important evolutionary force maintaining genetic variation in natural populations.

On elytral morphology, sexual conflict and female mating polymorphism in diving beetles: new paper in "Interface"

Posted by Erik Svensson

Forrmer PhD-student Kristina Karlsson-Green (currently postdoc in the "Metapopulation Research Group in Helsinkki, Finland) has published one of her last thesis-paper in the Royal Society Journal "Interface". This paper deals with a fascinating female mating polymorphism in diving beetles, where females have either a "rough" or "smooth" elytral morphology. She has quantified fine-scale female elytral morphology using scanning electron microscopy (SEM), as well as male morphological adaptations to clasp females during matings in the form of so-called "suction cups" (see picture above), and also used a biomechanical experiments to quantify male adhesion ability on the different female morphologies.

Results provide experimental support to the suggestion that this female mating polymorphism is maintained by sexually antagonistic and frequency-dependent selection caused by sexual conflict, and different male phenotypes show different ability to clasp the different female morphs. The experiments in this fascinating study were performed in collaboration with our colleague Prof. Stanislav N. Gorb, at Kiel University (Germany), and I personally like this combination of biomechanics and evolutionary biology very much. Below, you find a link and Abstract to the study.

Male clasping ability, female polymorphism and sexual conflict: fine-scale elytral morphology as a sexually antagonistic adaptation in female diving beetles

1. Kristina Karlsson Green, 
2. Alexander Kovalev, 
3. Erik I. Svensson and
4. Stanislav N. Gorb

During sexual conflict, males and females are expected to evolve traits and behaviours with a sexually antagonistic function. Recently, sexually antagonistic coevolution was proposed to occur between male and female diving beetles (Dytiscidae). Male diving beetles possess numerous suction cups on their forelegs whereas females commonly have rough structures on their elytra. These rough structures have been suggested to obstruct adhesion from male suction cups during mating attempts. However, some diving beetle species are dimorphic, where one female morph has a rough elytra and the other has a smooth elytra. Here, we used biomechanics to study the adhesive performance of male suction cups on the female morphs in two diving beetle species: Dytiscus lapponicus and Graphoderus zonatus. We compared adhesion on the rough and the smooth female morphs to infer the function of the rough elytral modifications. We found that the adhesive force on the rough structures was much lower than on other surfaces. These findings support the suggestion of sexual conflict in diving beetles and a sexually antagonistic function of the rough female structures. In addition, males differed in their adhesive capacity on different female surfaces, indicating a male trade-off between adhering to smooth and rough female morphs.

Talk on frequency-dependent selection by Yuma Takahashi

Posted by Erik Svensson

Next week's lab-meeting will take place in "Argumentet" (2nd floor, Ecology Building) on Tuesday September 11  at 10.30, i. e. usual time. This time, it will be our postdoc Yuma Takahashi from Japan who will give a short and informal talk about his past and ongoing research on colour polymorphisms and frequency-dependent selection in Ischnura-damselflies. As some of you already know, Yuma did his PhD-research on the damselfly species Ischnura senegalensis, a tropical counterpart to Ischnura elegans, who we have been working on in Sweden and Europe. You can read more about Yuma's research here, and find his publications here.

Do not miss this opportunity to listen to Yuma and his interesting research. I will bring some "fika".

Lab-meeting and some interesting evolutionary articles in Science

This week's lab-meeting will take place at an unusual time: Friday 9 December at 10.00 in "Argumentet". I hope you can make it, as Machteld and I will tell us a little bit about our impressions from the ASAB-meeting in London, where we recently participated. In addition, I would like to discuss two recent articles in Science which are of interest to evolutionary ecologists (and which are short reads). You will find more information about these papers below, including links and Abstracts.

First, there is this interesting study about negative frequency-dependent selection in voles: 

Negative Frequency-Dependent Selection of Sexually Antagonistic Alleles in Myodes glareolus

1. Mikael Mokkonen¹,*,
2. Hanna Kokko²,
3. Esa Koskela³,
4. Jussi Lehtonen²,⁴,
5. Tapio Mappes¹,
6. Henna Martiskainen³,
7. Suzanne C. Mills⁵

Abstract

Sexually antagonistic genetic variation, where optimal values of traits are sex-dependent, is known to slow the loss of genetic variance associated with directional selection on fitness-related traits. However, sexual antagonism alone is not sufficient to maintain variation indefinitely. Selection of rare forms within the sexes can help to conserve genotypic diversity. We combined theoretical models and a field experiment with Myodes glareolus to show that negative frequency-dependent selection on male dominance maintains variation in sexually antagonistic alleles. In our experiment, high-dominance male bank voles were found to have low-fecundity sisters, and vice versa. These results show that investigations of sexually antagonistic traits should take into account the effects of social interactions on the interplay between ecology and evolution, and that investigations of genetic variation should not be conducted solely under laboratory conditions. 

Second, there is this study on individual face recognition in paper wasps: 

Specialized Face Learning Is Associated with Individual Recognition in Paper Wasps

1. Michael J. Sheehan*,
2. Elizabeth A. Tibbetts

Abstract

We demonstrate that the evolution of facial recognition in wasps is associated with specialized face-learning abilities. Polistes fuscatus can differentiate among normal wasp face images more rapidly and accurately than nonface images or manipulated faces. A close relative lacking facial recognition, Polistes metricus, however, lacks specialized face learning. Similar specializations for face learning are found in primates and other mammals, although P. fuscatus represents an independent evolution of specialization. Convergence toward face specialization in distant taxa as well as divergence among closely related taxa with different recognition behavior suggests that specialized cognition is surprisingly labile and may be adaptively shaped by species-specific selective pressures such as face recognition.

Beyond the Fst-Qst comparison: Insights from the EGRU-blog

You are probably aware of the fact that there are many problems of Fst-Qst-comparisons to infer selection, and this method is also known to have weak statistical power. Essentially, this means that even if selection acts on a phenotypic trait, this method might not be able to detect it, and a finding that Qst equals Fst does not mean that selection is not operating on the trait in question. This low statistical power is a problem, because if one finds a positive result, one can always say that selection has operated on the trait of interest, but not much can be said if one finds a negative result. The trait might then be "neutral" and not subject to selection - or it might be subject to selection, but we cannot detect it with the current method.

There might be solutions and alternatives to the Fst-Qst-comparisons, however. At Juha Merilä's research group blog "EGRU-blog", he refers to a recently published theory-paper in Genetics, which seems like an interesting read. Although I have not read this paper in detail, it is a paper worth keeping in mind, and worth returning to in the future. I took the liberty to borrow the picture from Juha's blog and some of the text where he explains the main implications of their study:

"The main point here to note is that this method allows detection of signatures of selection also in the case where Fst =Qst: the selection in these cases (c,d) is inferred from the fact that population centroids tend to cluster according to selective regime (color) rather than their ancestry (shape of the symbol). It is also worth pointing out that the new method accounts for many other technical problems that have plagued traditional Fst-Qst comparisons. Read the paper and become enlightened!"

To this, I would like to add that it is unlikely that we will ever find the molecular method that can replace the vastly superior method of directly measuring natural or selection in the wild, or quantify quantitative genetic patterns that reveal the action of past selection. Observing something directly, and trying to quantify it, will certainly always reveal more about agents of selection and mechanisms, than indirect inferences like the Fst-Qst comparison.

This does of course not mean that these indirect methods should never be used. Far from it, and we have used such methods in the past in this,  this and this study of ours, for example. But these methods can only be a first step, and if selection is inferred, it should only be considered as a preliminary working hypothesis, that needs to be experimentally corroborated. And moreover, some forms of selection, such as negative frequency-dependent selection, might seldom, or never be detectable when there is weak genetic differentiation between populations (precluding the prospects of finding a pattern where Qst < Fst), and in these cases, direct experimental field studies might be the only possible option. There is never an excuse to avoid going out the field or doing experiments in evolutionary biology, if it is possible.

Lab-meeting on the ecology of (incomplete) speciation

This Wednesday(September 23), I was thinking that we should discuss the issue of incomplete speciation and "speciation reversal", i. e. the opposite of speciation. There is a recent TREE-article by Patrik Nosil, Luke Harmon and Ole Seehausen that deals with this issue, and which can be found here.

Personally, I think that the issue of why speciation does not occur, is as important as why it occurs, and hopefully we will learn something new from this article. I think that our study systems (lizards, isopods, damselflies) are almost perfect in many respects to adress these kind of fascinating questions, so please study this article in depth.

Time and place as usual: the "Darwin"-room at 10.00 on Wednesday September 23. Any fika-volunteer?