Adventures in Space & Time

Blog written by Dr. Tristan A.F. Long, Associate Professor at Wilfrid Laurier University, Canada. @thelonglab

Read the full paper here.

Sexual selection is a powerful agent for evolutionary change, as the patterns of non-random mating arising from male-male competition for mates and/or choosiness for mates on the part of females, can strongly determine who passes on their genes to the next generation, and who doesn’t (i.e. differential reproductive success of individuals). In our recently published paper [1] we set out to examine the role that spatial complexity in a species’ environment plays in shaping how males and females interacts and how this affects the operation of sexual selection.

It has long been recognized that changing the complexity of an environment can dramatically affect how natural selection (differential survival of individuals) can operate. For instance, in structurally simple environments, it may be easier for predators to detect prey, resulting in stronger selection on prey, than if the same species were located in a more structurally complex environment (where there are more places to hide). But is the same true for sexual selection? There are many different (and potentially conflicting) ways that more spatially complex environments can potentially change in the frequency and type of interactions between individuals. Conceivably, in a simpler environment, males might experience stronger selection arising from more frequent male-male interactions; however a complex environment might conceivably impose greater selective pressures on males as they search for potential mates.  When considering inter-sexual selection, females might be able to make better assessments of potential mates in a simple environment if they can be compared more easily and there are smaller sampling costs; however, if there is ultimately less male-male competition in complex environments, then there may be more opportunities for females to exert their mate preferences.

The nature of these changes in the interactions between males and females can be further complicated if there is intersexual conflict (which can result from differences between the sexes in their fitness‐maximizing strategies). In some species, this conflict can lead to males evolving traits and behaviours that benefit their own fitness through the manipulation of their mates, ultimately decreasing the females’ lifetime reproductive success.

With all these different possibilities in mind, we set out to conduct some empirical tests of the effect of manipulating spatial complexity. Our tests were conducted using fruit flies, Drosophila melanogaster. In our lab, like many others across the globe, populations of flies are maintained in vials – which obviously represents a very, very, very simple environment. With these ‘simple vials’ acting as the control treatment, we experimentally enhanced vial complexity by adding in a piece of acetate, folded accordion-style into the vial, which increased the amount of surface area within. This is, all things considered, a relatively minor change in structural complexity, but we didn’t want to place our experimental treatment flies into a wholly novel environment (different from the one in which the populations had been evolving), where we would be unable to conclude whether any changes we saw in reproductive interactions or their outcomes, were the result of the change in the structural complexity, or a response to some other aspect of the different environment.

FLY_VIALS
Examples of standard fly vials containing media (dyed green for increased visual contrast) and strips of acetate, folded accordion-style

In our experiment, we were interested in seeing the effects of the differences in environmental complexity on mating frequencies, the direct effects on female reproductive output, as well as whether there were any consequences of the environmental differences manifested in the females’ offspring. We speculated that if an increase in structural complexity made it harder for males to manipulate and harm their mates (in D. melanogaster, male courtship, mating and the products passed on in their ejaculates can all lead to shorter lifespan and lower lifetime egg production in females [2]), then we would see females directly benefitting from the complexity, and producing more offspring than those in simpler environments. If however, more complex environments imposed greater selection against males such that only those individuals of the best ‘quality’ could efficiently locate and mate with females, then one might predict that these effects would be manifested indirectly in the next generation, with the offspring sired in complex environments being more successful than those sired in simpler environments.

In each of our experiments, we combined male and female flies in either simple or complex vials, and left them to interact for between 1 and 4 days (to examine if these effects changed over time). In our first assay, we measured female offspring production, and, by first mating females to males carrying a dominant brown-eyed allele, we could measure initial remating rates by looking at the colours of her offprings’ eyes. We also conducted additional assays that compared the reproductive success of offspring that were sired in either environmentally simple or complex vials.

test-tubes
In our assays, when it came time to measure female fitness, individuals were housed overnight in a test-tube, and the number of adult offspring that developed in these tubes was counted ~14 days later.

Overall, we found that females housed in complex vials were slower to remate for the first time, and laid more offspring compared to those females in the simple environments. Together, this suggests that males had a harder time finding and harassing females in the complex environment, and with the reduction in the magnitude of the sexual conflict present, females were able to achieve greater fecundities than would be possible in simpler vials. Interestingly, we did not see any systematic differences in the fitness of either male or female offspring sired in the complex or the simple vials. This suggests that the indirect effects of changes in environmental complexity are minor, compared to the direct impact (at least in our study species/population). Our work complements some other recent studies [3] that have also examined how the local environment mediates how sexual selection and sexual conflict operates. Together, these studies are helping us to better understand the variety of ways in which non-random mating patterns arise, and their consequences for adaptive evolution.

old_lab
“Fly-pushing” is a collaborative endeavour, and required many hands and eyes. Many thanks to the Summer 2017 #DrosLife crew for all their hard work! (L:R) Kyle Schang, Heather Malek (MS 1st author), Renee Garant, Heather Jovanovic & Tijana Lazova (not pictured: Elvira Sathurni, Melvin Chen & Yvonne Young).

[1] Malek HL, Long TAF. Spatial environmental complexity mediates sexual conflict and sexual selection in Drosophila melanogaster. Ecology and Evolution. 2019.

https://doi.org/10.1002/ece3.4932

 

[2] Partridge L, Fowler K. Non-mating costs of exposure to males in female Drosophila melanogaster. Journal of Insect Physiology. 1990 Jan 1;36(6):419-25.

https://doi.org/10.1016/0022-1910(90)90059-O

Pitnick S, García–González F. Harm to females increases with male body size in Drosophila melanogaster. Proceedings of the Royal Society of London. Series B: Biological Sciences. 2002 Sep 7;269(1502):1821-8.

https://doi.org/10.1098/rspb.2002.2090

 

[3] Singh A, Agrawal AF, Rundle HD. Environmental complexity and the purging of deleterious alleles. Evolution. 2017 Nov;71(11):2714-20.

https://doi.org/10.1111/evo.13334

Yun L, Chen PJ, Singh A, Agrawal AF, Rundle HD. The physical environment mediates male harm and its effect on selection in females. Proceedings of the Royal Society B: Biological Sciences. 2017 Jul 5;284(1858):20170424.

https://doi.org/10.1098/rspb.2017.0424

Colpitts J, Williscroft D, Sekhon HS, Rundle HD. The purging of deleterious mutations in simple and complex mating environments. Biology letters. 2017 Oct 11;13(10):20170518.

https://doi.org/10.1098/rsbl.2017.0518

 

 

 

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