How do host sex and reproductive state affect host preference and feeding duration of ticks?

Abstract

Parasitism is one of the most notable forms of symbiosis in the biological world, with nearly all organisms hosting parasites. In many vertebrates, males have higher ectoparasite burdens than females, especially when testosterone concentrations are elevated. Furthermore, reproductive females may have higher ectoparasite burdens than non-reproductive females. It is possible that testosterone-stimulated behaviors in males and offspring investment by females incur energetic costs that inhibit immune function. If questing ticks can sense host sex or reproductive condition prior to attachment, they could potentially choose hosts with the poorest immune function, thereby leading to improved feeding success and decreased feeding duration. In this study, we examined the host-parasite relationship between western fence lizards (Sceloporus occidentalis) and the western black-legged tick (Ixodes pacificus) to test the following hypotheses: (1) ticks prefer male lizards to female lizards. (2) Ticks prefer male lizards with higher testosterone. (3) Ticks prefer reproductive female lizards to non-reproductive female lizards. (4) Ticks feed to repletion more rapidly (decreased feeding duration) on reproductive females and males with higher testosterone. In all three experiments, ticks failed to show a preference for one group over another as demonstrated by similar attachment rates between groups. This suggests that observed differences in ectoparasite loads in free-ranging lizards is due to some other factor than host choice. However, tick feeding duration on female lizards was shorter when hosts were reproductive, suggesting that host reproductive condition alters tick feeding, possibly due to a decreased immune response. Interestingly, ticks fed more slowly on male lizards with elevated testosterone, suggesting that testosterone may actually improve immune function against ectoparasites.