Evolutionary consequences of sex-biased resistance

Males and females often differ in the average parasite loads that they carry, and explanations for this pattern abound. For example, differences in size, stress levels, hormones (see here), exposure to parasites, and investment in defense have been shown to explain variation in parasite loads between the sexes. Such sex-biased parasitism has important implications for host behaviour and population dynamics, effects that in turn can ripple through the community. Non-surprisingly then, sex-biased parasitism is a recurrent topic in ecological parasitology; and yet, the evolutionary consequences of sex-dependent variation in resistance - following changes in parasite selection – are generally ignored.

At the same time as I was wondering about those evolutionary consequences of sex-biased resistance, I found myself in a laboratory full of guppies (Poecilia reticulata) coming from a series of field introductions that I initially intended to use for exploring female evolution of defense under relaxed selection (i.e. parasite removal – see here). This seemed like an excellent opportunity first to use the males that I was breeding in the lab, and second to have a go at the more general, and understudied, subject of sex independent evolution. During the last two decades, awareness of the extent to which novel environments and changes in biotic interactions may lead to rapid evolution has increased dramatically to the point in which this is now a common consideration in basic ecological studies, conservation efforts and management plans. Yet, one potential limitation of most studies is that they either focus on one sex or conflate both sexes as if they ought to experience the same level of selection and show the same response to selection. In all fairness, such an assumption might be acceptable in some instances, but should be carefully considered for sexually dimorphic traits or when the potential for sex-biased selection exists. And, of course, one such trait that may show such sex-independent responses to the same environmental change is at the core of my research interests: defence against parasites.

The extent to which males and females might evolve differently in response to the same environmental change is not straightforward, and thus worthy of exploration. On one extreme of a continuum, we might expect the sexes to show similar evolutionary responses given that they might experience a similar environment and share most of their genetic background. On the other extreme of the same continuum, we can expect the sexes to show different responses given that they could experience the same environment in different ways and differ in some important regions of their genome – as is well documented for myriads of behavioural, morphological and physiological sexually-dimorphic traits. Therefore, my collaborators and I decided to test whether male and female guppies  showing sexually dimorphic resistance to a common and deleterious ectoparasite (Gyrodactylus turnbulli) evolved following similar or divergent trajectories, after the experimental removal of said parasite in four replicate populations (Dargent et al. 2016).

First, we confirmed that resistance to Gyrodactylus differed between males and females from the (parasite-present) ancestral population used to seed the (parasite-free) introductions. Indeed, males had higher resistance than females, and this effect was not caused by males being smaller in size – and thus providing less surface area for Gyrodactylus to grow – than females. Second, as we showed previously (here), we found that females in the four Gyrodactylus-released introductions rapidly (4 and 8 generations) and repeatedly evolved increased resistance to the parasite. Interestingly, males did not evolve increased or decreased resistance in those same four and eight generations. Surprisingly, all four female populations shared the same evolutionary trajectories in resistance trait-space (i.e. they evolved in parallel) and towards the position of the ancestral male traits.

Although a potential argument could be that males evolve much more slowly than females, this does not seem to be the case here; males from these same populations have shown rapid evolution of other traits (e.g. colour – see here). Additionally, the explanations that we had outlined for female increased evolution of resistance (here) – that it was a pleitropic by-product of evolution in response to release from predation - does not hold well for males. Males in the source population experience stronger selection by predators than females, and therefore we would have expected to see an even larger increase in resistance. Having no clear selective explanations for the sex-specific evolution of resistance we consider the idea of stronger evolutionary constrains in males than in females. Put simply, either ancestral selection on resistance was stronger for males and depleted much of the available genetic variance, and thus constrained further evolution, or alternatively, the costs of increasing resistance are nonlinear making progress towards ever higher resistance progressively more costly.

Evolutionary trajectories of guppies in resistance trait-space (parasite intrinsic rate of increase (r) and peak load). (a) Females from the introduced populations (filled symbols) evolved increased resistance to Gyrodactylus spp. relative to ancestral females from the source population (S), while males  did not(empty symbols). Ellipses represent 75% data spread for females (b) and males (c).

Studies of sex-biased parasitism recognize that behavioural and physiological differences between the sexes can lead to divergent parasite loads, and nonetheless, these studies ignore the potential effects of sex-specific evolution on those traits that influence host infection levels. Our results show that sex-biased resistance is a highly dynamic character, and help clarify why it has been so challenging to establish general patterns and mechanisms of sex-biased parasitism.

The paper:

Dargent, F., Rolshausen, G., Hendry, A.P., Scott, M.E. & Fussmann, G.F. (2016). Parting ways: Parasite release in nature leads to sex specific evolution of defense. Journal of Evolutionary Biology, 29(1), 23-34.