Parting Ways: Parasite Release in Nature Leads to Sex-Specific Evolution of Defence
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doi: 10.1111/jeb.12758 Parting ways: parasite release in nature leads to sex-specific evolution of defence F.DARGENT*,G.ROLSHAUSEN†,A.P.HENDRY†,M.E.SCOTT‡ &G.F.FUSSMANN* *Department of Biology, McGill University, Montreal, QC, Canada †Redpath Museum, McGill University, Montreal, QC, Canada ‡Institute of Parasitology and Centre for Host-Parasite Interactions, McGill University, Montreal, QC, Canada Keywords: Abstract enemy release; We evaluated the extent to which males and females evolve along similar experimental evolution; or different trajectories in response to the same environmental shift. Specifi- Gyrodactylus turnbulli; cally, we used replicate experimental introductions in nature to consider Poecilia reticulata; how release from a key parasite (Gyrodactylus) generates similar or different resistance; defence evolution in male vs. female guppies (Poecilia reticulata). After 4–8 sexual dimorphism. generations of evolution, guppies were collected from the ancestral (parasite still present) and derived (parasite now absent) populations and bred for two generations in the laboratory to control for nongenetic effects. These F2 guppies were then individually infected with Gyrodactylus, and infection dynamics were monitored on each fish. We found that parasite release in nature led to sex-specific evolutionary responses: males did not show much evolution of resistance, whereas females showed the evolution of increased resistance. Given that male guppies in the ancestral population had greater resistance to Gyrodactylus than did females, evolution in the derived popula- tions led to reduction of sexual dimorphism in resistance. We argue that previous selection for high resistance in males constrained (relative to females) further evolution of the trait. We advocate more experiments considering sex-specific evolutionary responses to environmental change. responses to environmental change likely influence Introduction overall fitness and population performance. Awareness that populations can evolve rapidly when The extent to which males and females might show exposed to novel environments has increased dramati- different evolutionary responses to the same environ- cally over the last 15 years (Hendry & Kinnison, 1999; mental change is not at all certain (Hendry et al., 2006; Reznick & Ghalambor, 2001; Merila€ & Hendry, 2014). Butler et al., 2007). On the one hand, males and Indeed, ‘contemporary’ (or ‘rapid’) evolution is now a females in a given population experience a similar envi- common consideration in basic ecological studies, con- ronment and share most of their genetic background – servation and management plans, and efforts to suggesting they should show similar evolutionary improve human well-being (Hendry et al., 2010; Scho- responses. On the other hand, males and females can ener, 2011; Carroll et al., 2014). In most cases, these experience a given environment in different ways and considerations treat males and females together or anal- do not share their entire genome – suggesting they yse only one sex or the other. However, we here show might show different evolutionary responses. Moreover, how similar environmental changes can lead to sex- the sexes typically exhibit differences in a broad array specific responses through which males and females of behavioural, morphological and physiological traits, evolve along different trajectories. Such sex-specific and this sexual dimorphism can be extreme (Darwin, 1872; Hedrick & Temeles, 1989; Badyaev, 2002; Delph, 2005). It thus seems plausible that males and females Correspondence: Felipe Dargent, Department of Biology, McGill University, 1205 Dr. Penfield Av., Montreal, H3A 1B1, QC, Canada. can experience different selective pressures even Tel.: +1 514 835 4235; fax: +1 514 398 5069; e-mail: when they share the same spatial location. Although [email protected]. some studies have examined the sex-specificity of ª 2015 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY. J. EVOL. BIOL. 29 (2016) 23–34 JOURNAL OF EVOLUTIONARY BIOLOGY ª 2015 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY 23 24 F. DARGENT ET AL. evolutionary responses to environmental differences removed from the natural context, which could strongly (Hendry et al., 2006; Butler et al., 2007; Kitano et al., alter evolutionary trajectories. Valuable insights there- 2012), none has considered sex-specific responses to fore can be gained by combining these two approaches shifts in parasitism, which is the focus of our study. through experimental manipulations in nature, which Hosts that move into new environments are often are rare in general (Reznick & Ghalambor, 2005) and exposed to a new parasite community, which can lead seemingly absent for evolutionary responses to parasite to infections by new parasite species (Ostfeld & Kees- pressure. A very important feature of this methodologi- ing, 2000; Kelly et al., 2009; Mastitsky & Veres, 2010; cal hybrid – one in which we were especially interested Frankel et al., 2015). Movement to new environments – is that field manipulations assess evolutionary out- can also lead to the loss of some parasites, such as comes in the presence of complicating and covarying through sampling effects or the absence of other condi- factors typical of the natural world. Although the pres- tions required by parasites (e.g. definitive/final hosts) ence of these factors inevitably reduces the precision of (Torchin et al., 2003). These shifts in selection (gains or inferences regarding mechanisms, it greatly increases losses of parasites) should cause evolutionary responses the ability to infer what happens when environments by hosts, as has indeed been observed in many change in nature. instances (Schmid-Hempel, 2011). For example, popu- We implement this field experimental evolution lations that are more heavily parasitized often evolve approach by comparing guppies (Poecilia reticulata) from increased resistance (Marshall & Fenner, 1958; Roy & a source (ancestral) population where a common and Kirchner, 2000; Boots et al., 2009) – presumably deleterious parasite (Gyrodactylus spp) is present to their because infection reduces survival (Anderson & May, descendants in four independent parasite-absent experi- 1978), fecundity (Herre, 1993) or mating success mental field introduction (derived) populations. Ances- (Hamilton & Zuk, 1982). By contrast, populations that tral and introduction sites also differed in that the are less heavily parasitized can evolve reduced resis- ancestral site had high levels of guppy predators whereas tance (Duncan et al., 2011) – presumably because resis- the introduction sites were predator-free (as described in tance mechanisms can reduce fitness in the absence of more detail in the Materials and Methods, and Discus- parasites through immunopathology (Graham et al., sion). After 4–8 generations of evolution in these novel 2005; Sorci et al., 2013), physiological costs of main- environments, we used individual-level laboratory taining immune responses (Lochmiller & Deerenberg, infections to assess resistance to Gyrodactylus turnbulli. 2000) or antagonistic pleiotropy such as trade-offs with We previously analysed some data from this experiment, fecundity (Boots & Begon, 1993). showing that females rapidly and repeatably evolved To what extent will males and females evolve increased resistance to Gyrodactylus after this parasite is similarly or differently to such shifts in parasitism? On removed (Dargent et al., 2013a). This apparently coun- the one hand, the sexes can be similarly influenced by ter-intuitive result reveals the importance of performing parasites. As the genes that influence resistance are manipulations in nature because it shows how the out- often found on autosomes (Murphy et al., 2008), a shift comes typical of laboratory experiments can be strongly in parasite pressure might lead to similar evolutionary altered in the complex natural world. In this study, we responses in males and females. On the other hand, the delve further into the experiment to compare the evolu- sexes often experience different parasite levels, have tionary responses of males and females. different costs of infection, and can have different costs We organize our analysis around five questions of defence (Folstad & Karter, 1992; Zuk & McKean, (Table 1). First, we test for sexual dimorphism in resis- 1996; Forbes, 2007; Nunn et al., 2009). The result tance in the ancestral population because the initial state might be sex-specific evolutionary responses to shifts in will likely shape evolution in altered environments. parasitism. Our goal was to experimentally discriminate Second (for females) and third (for males), we explore between these two plausible alternatives. the extent to which resistance has evolved across the four replicate experimental introductions. Fourth, we evaluate sexual dimorphism in the derived populations, Our study thus informing how dimorphism has evolved from the Inferences regarding the evolution of parasite resistance ancestral state. Finally, we quantitatively compare the are usually based on field surveys (Jokela et al., 2003; evolutionary trajectories of males and females in the Bonneaud et al., 2011) or laboratory experiments trait space defined by two resistance traits. (Schulte et al., 2010; Duncan et al., 2011; Koskella et al., 2012). Although informative, these approaches are lim- Materials and methods ited in several respects. Field surveys are limited because it is difficult to (i) infer causation without experimental All field procedures were approved