How sexual conflict can drive the elaboration of a sexually dimorphic trait

Every so often, a scientific paper comes along that really ticks all the boxes: the science is exciting, the methods innovative, the outcome tells you something new, and it comes together to make a great story. The latest research from Locke Rowe’s lab at the University of Toronto, Canada, is one such paper. I’m a big admirer of Rowe’s work – his 1996 paper with David Houle on the ‘genic capture’ model is a great bit of theory which provides a conceptual solution to a very thorny problem, while his book on sexual conflict (with Goran Arnqvist) is a thorough examination of the subject, and is packed with enough examples of weird mating systems that I really have no excuse for being so rubbish at updating my other website. Oh, and Rowe made me explain my poster to him at the European Society for Evolutionary Biology conference in Tuebingen last year while he drank a beer and pretty much just laughed at my nervous, sweaty mumblings. So, in all: great guy.

The paper in question furthers Rowe’s research into sexual conflict, which is the idea that males and females of a single species can have conflicting strategies when it comes to optimising fitness. The most obvious example of sexual conflict in action is mating rate. Females often need to mate only once to fertilise eggs (in insects, females can often store sperm away for future fertilisation); not only do additional matings bring no fitness benefits, but they can actually have detrimental effects on the immune system. By way of contrast, males should gain fitness with each mating, as it should fertilise more eggs (and thus produce more offspring). Anyone with a passing interest in reading science blogs is likely to be aware of the kind of morphological terror that can occur when there’s conflict over the frequency of reproduction: that’s right, it’s time to link to Ed Yong’s seminal (hah) duck-genitalia article. Again.

This time, we’re taking a closer look at the murky world of those poster children for sexual conflict: water striders. Females don’t just resist their suitors due to the usual costs of mating; there is an additional reason for their vigorous struggles. Because males try to mount females atop the surface of the water, the female in particular is susceptible to death from below – a situation that has led to something of an evolutionary ‘arms race’ in terms of morphology and tactics in water striders as each sex aims for a fitness advantage.

Image by Chang S Han. Read Han’s paper with Piotr Jablonski – or just watch the video – about males intimidating females into sex by attracting the attention of predators here. Alternatively, check out the feature in Nature!Sex!TopTips!

The Rheumatobates genus of water striders is known for strange structural modifications in males, used as ‘graspers’ in order to overcome the vigorous resistance they come up against in females. This female resistance is so strong that only around 12% of mating attempts by males are actually successful, indicating just how much of a force sexual conflict is in this species. In this paper, Rowe and colleagues Abderrahman Khila and Ehab Abouheif were studying a particular species named Rheumatobates rileyi, in which the antennae of males are curious and elaborate structures. Through the use of high-speed video, flash-freezing mating pairs, and scanning electron microscopy, they were able to show that there are four composite traits in these antennae, perfectly adapted to grasp the female head. Just in case that passed you by: mating pairs of water striders were lobbed unceremoniously into liquid nitrogen in order to study exactly how these male graspers fit to female heads. Science is AWESOME. This was the first piece of the puzzle: to find some evidence suggesting that the structures are driven by sexual conflict, and that they are not simply for general grasping use by males (hint: look at the picture below).

A: close-up of male head
B: super-intense-close-up of the hook
C,D: female’s head, colour-coded to match where male grasping traits ‘lock’ in
E,F: male antennae grasping female head (two different positions)

Using superfancypants transcriptome sequencing technology, they determined that the gene ‘distal-less’ (dll) was responsible for causing males to develop all four grasping traits on their antennae. While dll is expressed in both male and female antennae, it has no such effect in females. By using a technique called RNA interference (RNAi) to disrupt the expression of this dll gene, they produced male water striders which had varying expression of these traits, from “complete loss to a subtle reduction”. They then put these males to work in trying to mate with normal females.

The results are clear to see: just as the antennal grasping traits are reduced, so follows the mating success. RNAi males with no difference from ‘wild type’ had similar success to the average water strider; those with mild reduction in grasping traits failed significantly more, and those with moderate reductions failed on more occasions (and more quickly) than that. These ‘moderate’ RNAi males failed so quickly because their antennae failed to keep hold of the female’s head during the initial flip.

Taken together, this shows how the elaboration of the antennae in one sex of a species has arisen: the conflict between male and female fitness ‘strategies’, the fitness advantage which drives the need for grasping traits, and the genetic basis underlying the antennal elaboration. As the authors conclude, the graded effect of dll RNAi and the corresponding consequences show that even slight modifications to an unmodified ancestral state (like the female antennae) should result in higher mating success, and thus higher fitness. As such elaborate graspers are found in multiple species within this genus, there is a good possibility that variation in the expression and function of the dll gene, combined with sexually antagonistic behaviour, underlies this diversity.

Read the full paper here:

Abderrahman Khila, Ehab Abouheif, Locke Rowe (2012) Function, Developmental Genetics, and Fitness Consequences of a Sexually Antagonistic Trait. Science 336, 585

Image 1 copyright Chang S Han
Image 2 copyright Science magazine
Image 3 copyright Science magazine; modified by me (that’s right, they didn’t actually publish it like that)


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