a Frontiers of Biogeography 2021, 13.2, e49428 Frontiers of Biogeography RESEARCH ARTICLE the scientific journal of the International Biogeography Society Biogeographic patterns of blood parasitism in the Aegean wall lizard (Podarcis erhardii) across the Cycladic Islands Johanna L. Fornberg1,2* and Sarah L. Semegen1 1 School of Natural Resources and Environment, University of Michigan, Ann Arbor, MI, 48104, USA; 2 Department of Ecology, Evolution, and Marine Biology, University of California - Santa Barbara, Santa Barbara, CA, 93117, USA. *Correspondence: Johanna Fornberg ([email protected]), Address: University of California Santa Barbara, Santa Barbara, CA, 93106, USA. Abstract Highlights The biogeography of host-parasite dynamics is an area • Land-bridge islands provide a natural study system that has received little attention in studies of island to explore the effect of island structure and ecology ecology. While a few studies have shed insight on patterns on native host-parasite interactions, such as the of parasitism in insular host populations, more empirical relationship of hemogregarine parasites and a lacertid evidence is needed to ascertain how isolation impacts lizard host, Podarcis erhardii, in the Cyclades. parasites. Biogeography generally theorizes that the physical size of islands and the duration of each island’s • We fit models of prevalence and parasitemia to isolation can be driving geographic factors controlling empirical observational data and demonstrated that species interactions and populations dynamics. To biological and geographical factors correlate with test this, we assessed the effect of island structure parasitism, and that biological and geographical and population isolation on the endemic insular lizard variables are interconnected in this context. Podarcis erhardii and its native hemogregarine parasite (Apicomplexa: Adeleorina) in the Cyclades (Aegean • This work suggests that isolation time and host Sea). We analyzed the relationships of prevalence and population density, in particular, are strong predictors parasitemia of hemogregarine infection with several of parasitism for native island hosts and that insular factors concerning the island (size, time of isolation, density compensation may be a mechanism for this spatial isolation, population density) and host (body size) pattern. levels using regression and structural equation models, respectively. Regressions indicate that islands with greater • Further exploration of insular host-parasite host density and islands which have been isolated for interactions will not only deepen our understanding shorter timespans tend to have higher hemogregarine of parasite ecology, but may also act as a valuable prevalences; structural equation models suggest a indicator for how habitat fragmentation may affect similar pattern for parasitemia. We hypothesize this may host-parasite dynamics in the future. be driven by insular density compensation. Hosts on islands that are more temporally and spatially isolated also tend to have higher prevalence and parasitemia of hemogregarines. Our results indicate that island area, island isolation, and host population density are likely to be significant drivers of changes in host-parasite interactions in fragmented populations. Keywords: Aegean Sea, biogeography, fragmentation, hemogregarines, host-parasite interactions, insularity, land-bridge islands, lizards. Introduction (MacArthur and Wilson 1967, Adler and Levins 1994, Blondel 2000, Blumstein and Daniel 2005, Research in island biogeography has uncovered Hurston et al. 2009, Novosolov et al. 2013), but less is a variety of ecological patterns and processes that known about the impact of insularity on host-parasite affect fragmented and isolated biotic communities. dynamics (i.e., infectious species which decrease host Many studies focus on the effect of fragmentation fitness with a pathology that is intensity-dependent, and insularity on community structure, physiology, Lafferty and Kuris 2002) (McCallum and Dobson morphology, and predator-prey interactions 2002). In a recent survey, biologists determined that e-ISSN: 1948-6596 https://escholarship.org/uc/fb doi:10.21425/F5FBG49428 © the authors, CC-BY 4.0 license 1 Fornberg & Semegen Blood parasitism in Aegean Wall Lizards one of island biology’s top research priorities was diversity and more apparent evolutionary divergence understanding how island isolation and size affected than islands that are less isolated but of the same size population dynamics (Patiño et al. 2017). (Simberloff and Wilson 1969, Simberloff 1976). Evidence has shown that isolation can have wide- The predictions of island biogeography theory have ranging impacts on host-parasite distributions and been developed for several decades in the context interactions (Perkins 2001, Morand and Krasnoz 2010). of free-living species, and little of this work has been Hosts may effectively lose parasites when isolated if extended to consider symbiotic species like parasites, host populations become small or dispersed (Clay 2003, pathogens, and mutualists. Insular communities Torchin et al. 2003), or parasites may evolve to have are, in some cases, depauperate of symbiotic a wider niche, thereby infecting new additional hosts species. Parasites, for example, may be entirely lost (Nieberding et al. 2006). Hosts may also be more in the process of isolation from the host species susceptible to parasitism if hosts are inbred, which (Torchin et al. 2003, Tomé et al. 2018). Loss or reduction could be determined by spatial and temporal isolation of symbiotic species may be a result of restrictions in trends (Reed and Frankham 2003, Charpentier et al. host species abundance, environmental or dispersal 2008). Parasitologists and ecologists have developed limitations, or a consequence of evolutionary changes theory detailing the possibilities of host-parasite in hosts, parasites, or both. For parasites infecting evolution following isolation, but there is still much isolated host species, we may expect that parasites opportunity for empirical and observational study of evolve to be less host specific over time as this may island biogeography in natural systems (Poulin 2004, be expected to increase transmission and abundance, Illera et al. 2015). however, a depauperate host population or low Generally, insular systems often exhibit higher immigration may reduce or prevent parasite survival. aggregate population densities on small islands Integrating parasitism into island biogeography theory as compared to larger islands and mainland requires a careful assessment of how free-living species areas, a process known as density compensation dynamics affect symbiotic species that operate at a (MacArthur et al. 1972, Wright 1980, Rodda and finer spatial scale than their hosts. Parasites (and other Dean-Bradley 2002). Studies that have investigated symbionts) are so intimately associated with hosts the relationships between parasitism and island that host individuals or populations are functionally biogeography suggest that isolation tends to lead equivalent to habitat and patches for parasite species smaller islands with denser host populations to harbor (Kuris et al. 1980, Combes 2001). higher parasite prevalence and infection intensity, The Cycladic islands are an archipelago of land- and lower richness of parasite diversity (Gouy de bridge islands in the Aegean Sea, located off the eastern Bellocq et al. 2002, Roca et al. 2009). While density coast of Greece (Fig. 1). Most of the islands, and the compensation is documented in faunal populations vertebrate populations inhabiting them, became (Wright 1980, Rodda and Dean-Bradley 2002), it progressively isolated during the gradual rise in sea is not clear how this process manifests in a host- levels following the last glacial maximum 18000 years parasite system when isolation also varies spatially ago (Pirazzoli and Pluet 1991, Kapsimalis et al. 2009, and temporally. Poulos et al. 2009). Duration of island isolation depends Related biogeography research suggests that on the depth of the underwater saddle between more intense isolation lead to a distinct loss of two islands and varies greatly between 25 years genetic diversity in the parasite and subsequently and 5.33 million years (Foufopoulos and Ives 1999). impoverished parasite populations in hosts (Reed Multiple lines of evidence indicate that the Aegean and Frankham 2003, Nieberding et al. 2006, Pérez- wall lizard (Podarcis erhardii, Reptilia: Lacertidae) Rodríguez et al. 2013, Koop et al. 2014). Two related is a very poor over-water disperser; as a result, the study found insular parasite populations to be evolutionary history of Cycladic populations reflects increasingly depauperate the longer the period of the fragmentation history of the islands they inhabit isolation from the mainland (Roca et al. 2009, (Foufopoulos and Ives 1999, Hurston et al. 2009). Pérez-Rodríguez et al. 2013). There is also evidence The resulting diversity of habitat and population that isolation leads to higher parasitism in inbred characteristics of the Cycladic islands present an populations (Charpentier et al. 2008, Luikart et al. excellent study system to investigate the long-term 2008, Chapman et al. 2009). Another study found effects of habitat fragmentation on the evolutionary that island hosts, compared to mainland hosts, had ecology of host-parasite interactions. significantly more parasitism as a result of reduced We determined how island geography and host genetic