Co‐phylogeography and comparative population genetics of the threatened Galápagos hawk and three ectoparasite species: ecology shapes population histories within parasite communities

Abstract

The theory of inclusive fitness provides a powerful explanation for reproductive altruism in social insects, whereby workers gain inclusive fitness benefit by rearing the brood of related queens. Some ant species, however, have unicolonial population structures where multiple nests, each containing numerous queens, are interconnected and individuals move freely between nests. In such cases, nestmate relatedness values may often be indistinguishable from zero, which is problematic for inclusive fitness-based explanations of reproductive altruism. We conducted a detailed population genetic study in the polygynous ant Formica exsecta, which has been suggested to form unicolonial populations in its native habitat. Analyses based on adult workers indeed confirmed a genetic structuring consistent with a unicolonial population structure. However, at the population level the genetic structuring inferred from worker pupae was not consistent with a unicolonial population structure, but rather suggested a multicolonial population structure of extended family-based nests. These contrasting patterns suggest limited queen dispersal and free adult worker dispersal. That workers indeed disperse as adults was confirmed by mark-recapture measures showing consistent worker movement between nests. Together, these findings describe a new form of social organization, which possibly also characterizes other ant species forming unicolonial populations in their native habitats. Moreover, the genetic analyses also revealed that while worker nestmate relatedness was indistinguishable from zero at a small geographical scale, it was significantly positive at the population level. This highlights the need to consider the relevant geographical scale when investigating the role of inclusive fitness as a selective force maintaining reproductive altruism.

Parasite co-structure: broad and local scale approaches

“…In part, these patterns may be due to the ability of some louse species to hitch-hike on hippoboscid flies. Whiteman et al (2007) showed how differences in natural history traits among parasites of the same host species could lead to testable predictions about the factors that influence among population genetic structure in parasites. In a parasite-multihost comparison, Prugnolle et al (2005) found that parasite migration was largely influenced by the most vagile host in the parasite's life cycle.…”

Are lice good proxies for host history? A comparative analysis of the Australian magpie, Gymnorhina tibicen, and two species of feather louse

“…However, this idea assumes vertical transmission of the parasite and sharing of ecological constraints between parasite and host. Empirical studies have shown that dispersal ability Whiteman et al, 2007) of lice underlies patterns of population structure. In addition, ecological constraints such as humidity (Carrillo et al, 2007) and size of host may restrict the distribution of a species of louse.…”

“…Although use of an identical gene fragment for lice would have been preferred, the non-coding region of the mtDNA in lice is AT rich and greatly reduced in length (Covacin et al, 2006). In contrast, COI has been shown to be a highly variable marker that is useful for intraspecific studies of invertebrate species (Heilveil and Berlocher, 2006;Whiteman et al, 2007).…”

“…Recently, several studies have demonstrated the usefulness of parasites as proxies for inferring history or ecology of the host (Nieberding and Olivieri, 2007). For example, genetic variation in parasites has been useful in determining recent history and demography in a threatened species of hawk (Whiteman et al, 2007). These studies comparing host and parasite phylogenies have revealed a number of patterns.…”

Lousy heirlooms: Lice help illuminate the recent evolutionary history of an Australian bird

“…At the molecular level, parasites tend to evolve more rapidly than their hosts. This is particularly germane to the lice of birds and mammals, which can exhibit greater phylogeographic (Whiteman et al, 2007) and phylogenetic (Hafner et al, 1994) divergence than their hosts. It has also been used effectively in exploring the biology of hosts with small (bottlenecked) populations, as in endangered right whales whose cyamid 'lice' populations harbor considerably greater genetic variability than their hosts (Kaliszewska et al, 2005).…”