Phylogeography and Prevalence of Hemoparasites (Apicomplexa: Eucoccidiorida) in Galápagos Marine Iguanas, Amblyrhynchus cristatus (Reptilia: Iguanidae).

Abstract

Simple SummaryIt is estimated that a vast diversity of parasites populate our planet, many of them still to be discovered. Blood parasites (hemoparasites) of the phylum Apicomplexa may infect both vertebrates and invertebrates. Here, we used molecular methods to characterize the diversity of hemoparasites in the emblematic Galápagos marine iguana. We examined major island populations of marine iguanas across the Galápagos archipelago, performing the largest biogeographical study on the topic in this species. In addition, ticks were collected from marine iguana’s body to screen for hemoparasites. Our genetic analysis revealed two distinct clusters of hemoparasites belonging to Hepatozoon and/or Hemolivia. The occurrence of hemoparasites differed dramatically across islands, indicating that some populations may have mechanisms to reduce infection rates. The infection status of ticks did not match with their marine iguana hosts, suggesting that this method cannot be used to reliably know whether or not marine iguanas are infected. Given that apicomplexan blood parasites may cause important zoonotic diseases, studies like this one focusing on the relationship between parasites, their hosts and transmitting vectors, may help to shed light on the underlying mechanisms that wild animals employ to cope with pathogen infection. Parasitism is among the most common forms of coexistence of organisms of different species. Hemoparasites live in the bloodstream of the host where they complete different life-cycle stages. Members of the phylum Apicomplexa constitute a large portion of all hemoparasites infecting reptiles and their parasite transmitting vectors, including arthropods. In this study, we carried out a survey and molecular identification of hemoparasites in blood samples of the iconic Galápagos marine iguana (Amblyrhynchus cristatus). Major island populations of marine iguanas were sampled to examine large-scale biogeographic patterns of parasite diversity and prevalence. Nested PCRs were used to amplify segments of the 18S rRNA-gene of hemoparasites. Furthermore, ticks attached to marine iguanas were collected and analyzed in the same way to assess their potential use as a non-invasive method for the detection of hemoparasites in vertebrate host species. PCR products were sequenced and a phylogenetic analysis was carried out showing the presence of two genetically distinct clusters of hemoparasites, one more commonly distributed than the other one, belonging to the genera Hepatozoon and/or Hemolivia (Apicomplexa: Eucoccidiorida). Overall, 25% of marine iguanas were infected by hemoparasites. However, infection rates varied strongly among particular island populations (from 3.45% to 50%). Although marine iguanas are an extremely mobile species that has colonized all islands in the Galápagos archipelago, parasite occurrence was not related to geographical distance, suggesting that dispersal behavior has a minor role in parasite transmission. On most islands, females tended to have higher infection rates than males, but this relationship was only significant on one island. Overall, ticks and marine iguanas had similar prevalence and diversity of parasites. However, the infection profiles of ticks and their corresponding hosts (marine iguanas) did not mirror one another, indicating that this method cannot be used reliably to assess marine iguana infection status. Interestingly, we found that hemoparasite prevalence in marine iguanas and ticks tended to be positively correlated across islands. Our results indicate that certain populations of marine iguanas may have special mechanisms and adaptations to cope with parasite infection. In addition, other factors such as vector density, anthropogenic-related activities or the immunological state of marine iguanas could potentially affect the striking variation in hemoparasite prevalence across island populations.