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.

Dr. Yuma Takahashi receives postdoctoral scholarship from Japan to join our lab

I am pleased to announce that Dr. Yuma Takahashi from Japan has been awarded a three-year postdoctoral scholarship, and will join our laboratory in 2012. Yuma received his doctorate degree at University of Tsukuba and in his thesis work he studied female colour polymorphism, frequency-dependent selection and evolutionary dynamics of the damselfly Ischnura senegalensis. You can read more about Yuma's research here. His study organism (I. senegalenis) is a small coenagrionid damselfly is closely related to Ischnura elegans, which we have studied in our lab.

There are many interesting similarities, but also difference between these two polymorphic species. One major difference, though, is that Ischnura senegalensis has only two female morphs, not three as in Ischnura elegans. Another interesting ecological difference is that the male mimicking androchrome females are often in minority in I. senegalensis, or at least not much more than 50 % of the female population, whereas this female morph is often the most common morph in I. elegans (at least in Sweden where we have mainly studied it). These interesting ecological species differences will hopefully be understood better and be explored after Yuma joins our lab in 2012.

Yuma has already published eight papers from his thesis-work and here I would just like to point to his latest one, which recently appeared in the journal Evolution. Using a powerful combination of field observations and experiments and simulation modelling, they elegantly illustrated the evolutionary dynamics of this polymorphic system which strongly suggest that this dynamic is most likely the result of frequency-dependent sexual conflict interactions, caused by male-female antagonistic mating interactions. In short: males develop a "search image" for common female morphs, and common morphs become differentially sexually harassed, resulting in an inverse relationship between a morph's fitness and its frequency in the population, which leads to negative frequency-dependent selection (NFDS), a very powerful evolutionary mechanism to maintain genetic polymorphisms. 

These findings and conclusions by Yuma and his co-workers are very similar to our paper on I. elegans that we published in 2005 in American Naturalist. It is of course nice to see that the genus Ischnura continues to generate interesting studies and inspire evolutionary biologists in different countries, including Japan. As an aside, the next international dragonfly conferences (WDA) will also take place in Japan, south of Tokyo between July 31 and August 5 2011. I am very happy and flattered to become invited as a plenary speaker to this rather small meeting of odonate enthusiasts, amateurs, naturalists and researchers.

Below is the Abstract and link to Yuma's article in Evolution, for those who are interested in reading more about this fascinating species and study system:

Negative frequency-dependent selection in female colour polymorphism of a damselfly (Evolution 2010 64: 3620-3628)

Takahashi, Yuma, Yoshimura, Jin), Morita, Satoru) & Watanabe, Mamoru

Abstract: Negative frequency-dependent selection (NFDS) is one of the most powerful selective forces maintaining genetic polymorphisms in nature. Recently many prospective cases of polymorphisms by NFDS have been reported. Some of them are very complicated, although strongly supportive of the NFDS. Here we investigate NFDS in wild populations of the dimorphic damselfly Ischnura senegalensis, in which females occur as andromorphs and gynomorphs. Specifically, we (1) test fitness responses to morph frequencies, (2) built a simple population genetic model, and (3) compare the observed and predicted morph-frequency dynamics. Fitnesses of the two morphs are an inverse function of its own frequency in a population, and are about equal when their frequencies are similar. Thus the conditions necessary for NFDS are satisfied. The long-term field surveys show that the morph frequencies oscillate with a period of two generations. Morph frequencies in a small population undergo large oscillations whereas those in a large population do small oscillations. The demographic properties of the observed dynamics agree well with those of our model. This example is one of the simplest confirmed cases of NFDS maintaining genetic polymorphisms in nature.