It’s often important to know how frequently parasites are transmitted among hosts of the same species (intraspecific transmission) or among hosts of different species (interspecific transmission). But observing parasite transmission events can be very difficult in wildlife populations, so we often have to use proxies instead of measuring transmission rates directly. For instance, we might use the frequency with which two bird species share a nesting site as a proxy for how frequently we think that transmission should happen between the two species.
But of course, transmission doesn’t necessarily happen when two species contact each other. So how can we determine whether interspecific transmission is really happening? There’s more than one method, but today, I just want to talk about a cool method that I’ve seen in a bunch of recent papers: comparisons of parasite population genetic structure within and among host species. If parasite populations are highly genetically differentiated among host populations or among host species (or even among individual hosts!), then there is evidence for low parasite transmission and thus genetic mixing among host populations or among host species (or individual hosts). Conversely, if there is no genetic differentiation in parasite populations among host populations or host species, then there may be high parasite transmission among host populations or host species. Here are a whole bunch of examples of how this idea has been explored in the literature recently:
Ectoparasitic flies on bats (Olival et al. 2013):
Olival et al. (2013) sampled bat flies on three species of bats in the Pteropus genus at eight sites in Malaysia, Cambodia, and Vietnam. Almost all of the bat flies were from a single species: Cyclopodia horsfieldi. An analysis of the molecular variance in the sampled bat flies showed that very little of the variation was explained by geographic region or host species. This suggests high rates of interspecific transmission of this bat fly species among the three Pteropus bat species. Previously, interactions between the three bat species, including roost sharing, were thought to be uncommon. But because the bat flies pupate off the host in the roosts, Olival et al. (2013) suggest that perhaps interspecific transmission can happen when the different bat species share the same roost locations sequentially, rather than at the same time.
Even though there was low genetic structuring in the sampled Cyclopodia horsfieldi bat flies, for one bat host species (Pteropus hypomelanus), there was relatively low gene flow in the parasite population at some isolated island sites. It turns out that bat gene flow is also low at those smaller, more isolated island sites. But if that’s the case, then why don’t those parasites have distinctly different genetic lineages from other sites and host species? Olival et al. (2013) suggest that one of the bat species, Pteropus vampyrus, visits those more isolated island populations of Pteropus hypomelanus during long-distance dispersal, and that those visits provide enough population mixing to prevent divergence in the parasite lineages among sites and host species.
Ectoparasitic mites on bats (van Schaik et al. 2014):
Let’s stick with bats, but shift our geographic focus to central Europe and our parasite focus to mites in the genus Spinturnix. S. myoti mites live on Myotis myotis bats and S. bechsteini mites live on Myotis bechsteinii bats. Both mites have similar life histories, and they are only transmitted during direct contact; they can only survive for a few hours off a host bat, unlike the bat flies discussed above. S. myoti mites had high genetic diversity and panmictic genetic structure, with no differentiation among bat populations. S. bechsteini mites had low genetic diversity and high differentiation among bat populations. van Schaik et al. (2014) suggest that the differences in the genetic structure of the two mite species can be explained by the differences in the social systems of the two bat species. Myotis myotis bats have larger colony sizes, more inter-colony visits during the maternal season, and closer intraspecific associations during the mating season, and all of these factors could lead to more intraspecific transmission of S. myoti mites, both within and among colonies. That is so cool! (By the way, check out this post for more information about the relationship between host contacts and parasite transmission.)
Ectoparasitic flies on birds (Levin and Parker 2013):
In the Galapagos, great frigatebirds (Fregata minor) are parasitized by Olfersia spinifera hippoboscid flies, and Nazca boobies (Sula granti) are parasitized by Olfersia aenescens hippoboscid flies. The great frigatebirds have distinct genetic population structure among islands, but their hippoboscid flies and a pathogen transmitted by the flies (Haemoproteus iwa) have no genetic differentiation among islands (Levin and Parker 2013). Also, of the few Olfersia spinifera hippoboscid flies sampled on a second frigate species (F. magnificens), all flies had the most common fly haplotype on great frigatebirds. Similarly, the Nazca boobies had distinct genetic lineages among sites, whereas the hippoboscid flies on boobies showed no genetic differentiation among sites or among multiple booby host species.
So, what’s going on? How could the parasites be so well-mixed among sites, while their bird hosts are not? Levin and Parker (2013) suggest two hypotheses: 1) maybe alternative host species that weren’t considered in this study are doing lots of island hoping and carrying flies around with them. Remember that Pteropus vampyrus bats may play that kind of role in the bat fly example above. 2) Host genetic structure is distinct among islands because the birds are philopatric; they like to mate at their natal breeding site. But juvenile birds may still visit other sites without mating, and thus without influencing bird population genetic structures, and those visits could spread the parasites among the islands, thus mixing the parasite lineages.
Feather lice on birds (Koop et al. 2014):
Let’s stick with birds in the Galapagos, but let’s change our focal host to hawks (Buteo galapagoensis) and our focal parasites to feather lice (Degeeriella regalis). Hawks are thought to cross open water far less often than the frigatebirds and boobies in the previous example. Unsurprisingly, Galapagos hawk populations have high genetic differentiation among islands, where the genetic differences among populations increase with the distance among islands (Koop et al. 2014). Hawk feather lice also show high genetic differentiation among islands, unlike in our previous parasite examples. This suggests that there is very little interpopulation dispersal of lice, and there isn’t an alternative host carrying lice to different islands, either. Furthermore, lice are mostly vertically transmitted from parent to offspring, rather than the host-roost-host or horizontal host-host transmission routes in the previous systems. As a result, there is also genetic differentiation of lice among individual hosts, so that each host acts like a parasite island! Neat!
Feather mites on birds (Dabert et al. 2015):
Birds again, but now let’s talk about feather mites on two species of skuas (arctic and long-tailed skuas) in Svalbard. The mites are thought to be transmitted only during direct host contact, either vertically from mother to offspring or horizontally among hosts. Even though the two skua species nest at the same sites during the breeding season, nests tend to be spaced far apart, so Dabert et al. (2015) predicted that the two skua species would have distinct mite species. Both skua species had mites in the Alloptes genus, which were morphologically very similar, but which were genetically distinct enough between the two host species to be classified as two different species. However, both skua species also had Zachvatkinia isolata mites, and those mites had a well-mixed population with no evidence for genetic differentiation among host species. How could that be? Well, the two skua species do contact each other, during very brief but common aerial fights. And it may be that Zachvatkinia isolata mites, which are more abundant on the host and specialize on a relatively external region of the feathers, are more likely to be transmitted during those brief aggressive encounters than the Alloptes mites that hang out in more protected parts of the plumage. UHM, AWESOME.
You might be wondering if similar studies have been done with host species that don’t fly, or with endoparasites instead of ectoparasites. There is some endoparasite work, like with schistosomes and whipworms, but I’m not going to cover it here. As for non-flying host species, check back next week for an example of how the insight gained from studies like this can be used in an applied way to manage parasite transmission.
(I was watching a lot of Fringe when I made this cartoon.)
Dabert, M, SJ Coulson, DJ Gwaizdowicz, B Moe, SA Hanssen, EM Biersma, HE Pilskog, and J Dabert. 2015. Differences in speciation progress in feather mites (Analgoidea) inhabiting the same host: the case of Zachvatkinia and Alloptes living on arctic and longtailed skuas. Exp Appl Acarol 65:163–179.
Olival, KJ, CW Dick, NB Simmons, JC Morales, DJ Melnick, and K. Dittmar. 2013. Lack of population genetic structure and host specificity in the bat fly, Cyclopodia horsfieldi, across species of Pteropus bats in Southeast Asia. Parasites & Vectors 6:231
Koop, JA, KE DeMatteo, PG Parker, and NK Whiteman. 2014. Birds are islands for parasites. Biology Letters 10: 20140255.
Levin, II, and PG Parker. 2013. Comparative host–parasite population genetic structures: obligate fly ectoparasites on Galapagos seabirds. Parasitology 140: 1061–1069.
van Schaik, J, G Kerth, N Bruyndonckx, and P Christe. 2014. The effect of host social system on parasite population genetic structure: comparative population genetics of two ectoparasitic mites and their bat hosts BMC Evolutionary Biology 14:18.