The lifetime of a species: how parasitism is changing Darwin's finches

Sonia Kleindorfer, Jody A. O’Connor, Rachael Y. Dudaniec, Steven A. Myers,Jeremy Robertson, and Frank J. Sulloway. (2014). Species Collapse via Hybridization in Darwin’s Tree Finches. The American Naturalist, Vol. 183, No. 3, pp. 325-341

Small Galapagos tree finch,
Camarhynchus parvulus

Darwin’s finches are some of the best-known examples of how ecological conditions can cause character displacement and even lead to speciation. Continuing research on the Galapagos finches has provided the exceptional opportunity to follow post-speciation communities and explore how changes in ecological processes affect species and the boundaries between them. Separate finch species have been maintained in sympatry on the islands because various barriers maintain the species' integrity, preventing hybrids from occurring (e.g. species' behavioural differences) or being recruited (e.g. low fitness). As conditions change though, hybrids may be a source of increased genetic variance and novel evolutionary trajectories and selection against them may weaken. Though speciation is interesting in its own right, it is not the end of the story: ecological and evolutionary pressures continue and species continue to be lost or added, to adapt, or to lose integrity.

A fascinating paper by Kleindorfer et al. (2014) explores exactly this issue among the small, medium, and large tree finches (Camarhynchus spp.) of Floreana Island, Galapagos. Large and small tree finches first colonized Floreana, with the medium tree finch speciating on the island from a morph of the large tree finch. This resulted in three sympatric finch species that differ in body and beak size, but otherwise share very similar behaviour and appearance. However, ecological and environmental conditions have not remained constant on Floreana since observations in the 1800s: a parasite first observed on the island in 1997, Philornis downsi has taken residence and has caused massive nestling mortality (up to 98%) for the tree finches. Since parasite density is correlated with tree finch body size, the authors predicted that high parasite intensity should be linked to declining recruitment of the large tree finch. If females increasingly prefer smaller mates, there may also be increased hybridization, particularly if there is some advantage in having mixed parental ancestry. To test this, the authors sampled tree finch populations on Floreana in both 2005 and 2010. Parasite numbers increase with high precipitation, and so by combining museum records (collected between 1852-1906, when no parasites were present), 2005 sampling records (dry conditions, lower parasite numbers), and 2010 sampling records (high rainfall, high parasite numbers), they could examine a gradient of parasite effects. They measured a number of morphological variables, collected blood for genotyping, estimated individual age, measured parasite intensity in nests, and observed mate choice.

Philornis downsi:
larval stage parasitizes nestlings.
(a Google image search will provide
some more graphic illustrations)

For each time period, morphological measurements were used to cluster individuals into putative species. The museum specimens from the 1800s had 3 morphologically distinguishable populations, the true small, medium and large tree finch species usually written about. In 2005 there were still 3 distinct clusters, but the morphological overlap between them had increased. By 2010, the year with the highest parasite numbers, there were only two morphologically distinguishable populations. Which species had disappeared? Although recent studies have labelled the two populations as the “small” tree finch and “large” tree finch, the authors found that the 2010 “large” population is much smaller than the true large tree finches collected in 1852-1906, suggesting perhaps the large tree finch was no longer present. Genetic population assignment suggested that despite morphological clustering, there were actually only two distinct species on Floreana in 2005 and 2010: it appeared that the large tree finch species had gone extinct, and the boundary between the small and medium tree finch species had become porous, leading to morphologically intermediate hybrids.

The question then, is whether the extinction of the large tree finch and the collapse of the boundary between small and medium tree finches can be attributed to the parasite, and the changing selective pressures associated with it. Certainly there were clear changes in size structure (from larger birds to smaller birds) and in recruitment (from few young hybrids to many young hybrids) between the low parasite year (2005) and the high parasite year (2010). Strikingly, parasite loads in nests were much lower for hybrids and smaller-bodied populations than for the larger-bodied population (figure below). Compared to their large-bodied parents, hybrids somehow avoided parasite attack even in years with high parasite densities (2010). When parasite loads are high, hybrid offspring have a fitness advantage, as evidenced by the large number of young hybrids in 2012. The collapse of the large tree finch population is also likely a product of parasite pressures as well, as females selected smaller mates with comparatively lower parasite loads. Despite the apparent importance of the parasites in 2010, the existence of only a few older hybrid individuals, and greater morphological distance between populations seen in the 2005 survey (a low parasite period) suggests that selection for hybrids varies greatly through time. Though the persistence of the Philornis parasite on Floreana may prevent re-establishment of the large tree finch, changing parasite densities and other selective pressures may continue to cause the boundaries of the remaining finch populations to overlap and retract in the future. The story of Darwin's finches is even more interesting if we consider that it doesn't stop at character displacement but continues to this day.

From Kleindorfer et al 2014: Philornis parasite intensity in nests sampled in 2005 (lower parasite) and 2010/2012 (higher parasite), for nests of the small-bodied (population 1), intermediate hybrid, and larger-bodied (population 2) individuals.

INTECOL & the future of community ecology for infectious diseases – August 21st 2013 - #INT13

This year's conference has a strong focus on infectious disease which included today's symposium Community ecology for infectious diseases organized by Joanne Lello.

Throughout the symposium a great deal of interesting questions related to host-parasite interactions being addressed with a diverse set of methods ranging from the mathematical biology of Andy Dobson, to the experimental C. elegans / pathogenic bacteria systems of Olivier Restif and Gregg Hurst, the wild rodent systems of Heike Lutermann, Andy Fenton, and Owen Petchey, and the next generation molecular techniques employed by Serge Morand.

However, it was Robert Poulin the keynote speaker who set the theme of the symposium to which many of the speakers kept returning: What are the future directions of parasite community ecology? Dr. Poulin began the session with an overview of the recent trends in parasite ecology over the last few decades and Lawton's view that community ecology is a mess (Oikos 1999 – 84: 177-192). The initial research done on host-parasite interactions was centred within the one host – one parasite framework, often dealing solely with the effect of the parasite on its host. This was then expanded to the one host – multi-parasite level, often investigating drivers of parasite species richness among hosts via comparative analyses and occasionally extending to parasite-parasite interactions though the use of null models. Although the data were available beforehand, only recently has the field moved into the domain of multi-host – multi-parasite interactions, now focusing on questions of infection dilution, meta-analyses of parasite richness, and describing the networks of interactions within these communities.

Looking ahead into the future of this discipline, Poulin suggested that researchers should expand beyond simple topological networks of associations to include the strength of interactions, potentially via energy flow, and the use of network analyses on smaller scales using individual hosts. Serge Morand also highlighted the need to develop and incorporate parasite phylogenies into these multi-host - multi-parasite communities. His talk highlighted recent advances in next generation sqeuenceing and how these techniques can be applied to parasite communities. One obvious advantage is that through molecular phylogenetics researchers will be able to define and quantify a higher degree of parasite diversity, but additionally molecular markers can be used to uncover unexpected host diversity or identify species that may be difficult to distinguish through traditional taxonomic keys. Morand continued to press the application of new techniques in immunogenetics and the integration of methods in molecular epidemiology with the theory of transmission and community ecology.

Finally Andy Dobson posited that in addition to pressing forward with our research into infectious disease, it is imperative that contemporary researchers revist the “best hits” of the past and address important issues that have fallen to the wayside. Primarily Dobson pointed out that mathematically, aggregation and virulence of parasites have been shown as important factors for determining parasite co-existence. However, the concept of aggregation is often left out of contemporary discussions although it will be important to determine natural forms of the aggregation distribution and also to attempt to make the link between immunity and aggregation of parasites in a multi-host – multi-parasite community.

Whether incorporating novel molecular and statistical techniques, exploring previously unstudied model systems, or revisiting the context of contemporary research, it is clear that community ecology and infectious disease has a promising future and that it has progressed greatly from the mess Lawton made it out to be in 1999.