Coevolution of parasite virulence and host mating strategies

Abstract

Parasites are thought to play an important role in sexual selection and the evolution of mating strategies, which in turn are likely to be critical to the transmission and therefore the evolution of parasites. Despite this clear interdependence we have little understanding of parasite-mediated sexual selection in the context of reciprocal parasite evolution. Here we develop a general coevolutionary model between host mate preference and the virulence of a sexually transmitted parasite. We show when the characteristics of both the host and parasite lead to coevolutionarily stable strategies or runaway selection, and when coevolutionary cycling between high and low levels of host mate choosiness and virulence is possible. A prominent argument against parasites being involved in sexual selection is that they should evolve to become less virulent when transmission depends on host mating success. The present study, however, demonstrates that coevolution can maintain stable host mate choosiness and parasite virulence or indeed coevolutionary cycling of both traits. We predict that choosiness should vary inversely with parasite virulence and that both relatively long and short life spans select against choosy behavior in the host. The model also reveals that hosts can evolve different behavioral responses from the same initial conditions, which highlights difficulties in using comparative analysis to detect parasitemediated sexual selection. Taken as a whole, our results emphasize the importance of viewing parasite-mediated sexual selection in the context of coevolution.host-parasite coevolution | mate choice | virulence | transmission avoidance | sexually transmitted infection S ince Hamilton and Zuk (1) first proposed that parasitism may explain the existence of secondary sex traits such as the peacock's tail, there has been considerable interest in the role that parasites play in sexual selection and the evolution of mating strategies (2-19). A prominent theory, known as the transmissionavoidance hypothesis, posits that secondary sex traits, and more generally, mating strategies, have evolved to limit the risk of contracting an infection (10). Although this theory emphasizes the importance of parasites in determining mating strategies, it is clear that different mating strategies will have an impact on infectious disease transmission and therefore influence parasite evolution. However, despite this clear interdependence we lack a coevolutionary theory of mating strategies that captures reciprocal adaptations by both species.Sex can leave individuals at risk of infection due to sustained close contact with sexual partners or through the transfer of genetic material (20). Hence, sexually transmitted infections, which are common in both plants (21) and animals (22), are likely to be a key factor in the evolution of mating strategies. Furthermore, sexually transmitted infections typically exhibit different epidemiological dynamics (17, 23) and disease outcomes (e.g., sterility rather than mortality; ref. 22) to other in...

Host behaviour–parasite feedback: an essential link between animal behaviour and disease ecology

“…Parasites may manipulate host behaviour to enhance their own fitness, or changes in host behaviour may result from immunological or pathological consequences of parasite infection [6][7][8]. On longer timescales, parasites impose selective pressures on their hosts that can drive evolutionary changes in behaviour [9,10]; and in turn, these changes in host behaviour can shape parasite population dynamics and life history including traits such as virulence and transmission mode [11]. Ultimately, behaviour and parasitism are so tightly intertwined that we often cannot understand one without considering the other.…”

An ecological role for assortative mating under infection?

“…This applies a selection pressure on the pathogen towards lower virulence, so as not to impact the reproductive potential of the host too greatly. Supporting evidence for this comes from recent modelling work that suggests for the first time that all interactions between pathogens and host mating systems should be viewed as entirely co-evolutionary (Ashby and Boots 2015). This is a sea change in our understanding of how diseases impact their host mating systems and presently coevolutionary interactions are not widely incorporated into epidemiological models of disease spread.…”

Female assessment of male functional fertility during mate choice in a promiscuous fish

“…Disease‐infected males may also have lower functional fertility (Kekäläinen, Pirhonen, & Taskinen, ). In support of this hypothesis, a recent coevolutionary parasite‐host model (Ashby & Boots, ) predicts that female preference for healthy males is favoured and will evolve as a female mating strategy to avoid infection by transmittable parasites from diseased males. To date, there exist only a handful of studies reporting empirical evidence for female avoidance of recently mated males (Harris & Moore, ; Loyau et al., ; Markow, Quaid, & Kerr, ; Mellan, Warren, Buckholt, & Matthews, ; Nakatsuru & Kramer, ; Sato & Goshima, ; Scarponi, Chowdhury, & Godin, ).…”

“…If female guppies are not sperm limited, then their avoidance of males who they have recently observed mating, or otherwise sexually interacted, with another female in preference for unmated males (Scarponi et al, 2015) cannot be explained solely as an avoidance of recently mated males because of their depleted sperm stores per se (Sheldon, 1994). A plausible alternative functional explanation for such discrimination behaviour is that females might avoid previously mated males to minimize incurring other potential costs associated with mating with these males, such as increased risks of transmittable parasitic infection (Ashby & Boots, 2015;Houde, 1997;Sheldon, 1993) and physical injury to their gonopodial pore and tract (Langerhans, 2011), for example.…”