UCM Research group Vertebrate Biology and Conservation: Research

Implications of cryptic diversity of avian malaria parasites

Infectious diseases as biodiversity threats

Emerging infectious diseases represent a serious threat to human and wildlife health, as well as an important problem for the conservation of biodiversity. During the last decades, research on infectious diseases has incorporated evolutionary theory as a framework, both to interpret disease dynamics and to anticipate their consequences for populations.

One of our research lines explores the interface between host-parasite evolution and the analysis of disease threats in conservation biology. To realize this major purpose, we try to identify situations in which diseases pose a threat to biodiversity. For example, we study the effects of parasitism on small host populations, the consequences of parasite introduction for naive host species, and the importance of host migrations as pathways for disease spread across geographic regions.

Why is parasite diversity important?

Parasite diversity is a cornerstone of host-parasite relationships, which become more complex with increasing numbers of participating actors. For example, if a host species interacts with many parasite species, its immune system is likely affected by more natural selection pressures than if it interacts with just a few parasite species.

Cryptic diversity of avian malaria parasites

Malaria parasites, using a broad evolutionary definition, embrace the genera Plasmodium and Haemoproteus [1], a diverse group of protozoans that infect mammals, birds and reptiles, and are transmitted through the bite of various blood-sucking insects. A few hundred species have been described by examination of different morphological traits of these microscopic organisms. However, recent studies based on parasite identification by means of DNA sequence differences have revealed a much higher diversity of malaria parasites (Figure 1). Thus, only in birds, this group could include up to 10,000 distinct species [2].

Figure 1. Haemoproteus parabelopolskyi is a parasite species that can be distinguished by microscopy. However, a closer inspection reveals 24 different parasite lineages within such species, most of them specific to a single bird host species (represented with different colours). This is a particularly interesting case because it represents a mode of parasite diversification newly discovered for malaria parasites: within-host speciation of parasites [3].

Is it that important to take cryptic parasite diversity into account?

Our research has focused on the implications of cryptic parasite diversity. Up to now, we have shown that most parasite lineages, even if they differ by as little as 0.2% sequence divergence, qualify as biological species. Several lines of evidence led us to such conclusion:

Firstly, there is nearly total concordance between parasite phylogenies obtained from mitochondrial markers (a fragment of the cytochrome b gene) and from nuclear markers (a fragment of the DHFR-TS gene). This result suggests that these parasite lineages hardly recombine both genomes, and therefore can be considered to be reproductively isolated [2] [3].

We have observed that, despite of their genetic similarity, many parasite lineages demonstrate strong host specificity. For example, two sister parasite lineages (which differ by 0.2% sequence divergence at the cytochrome b) have been observed to remain nearly completely restricted to one bird species each (the melodious Hippolais polyglotta and the icterine H. icterina warblers), even though transmission to the other species is possible [4].

Besides, we have found important phenotypic differences among closely related parasites. Thus, parasites of blackcaps (Sylvia atricapilla), many of which are very similar genetically, show differences in phenology of transmission: some parasites are transmitted seasonally in breeding grounds, while others are transmitted all around the year [5]. In relation to their time of transmission, parasites also differ in their ability to disperse among host populations, as well as in their ability to locally infect hosts in the populations they colonise (Figure 2).

Figure 2. Malaria parasites of blackcaps show great phenotypic variation, as shown by their different dispersal potential and their rate of local transmission [5].

We also showed that understanding cryptic diversity in this group of parasites can be critical for revealing fundamental aspects of host-parasite interactions. For example, in the house sparrow Passer domesticus we have observed that the genetic background of the host, for example its alleles at the major histocompatibility complex, which are related to host's ability to recognise different pathogens, can make it resistant or susceptible to certain parasite lineages [6].

Future perspectives

Our research demonstrates that, if we are to understand the interactions between birds and their malaria parasites, we need a good control of the cryptic (genetic) diversity of parasites. Now we are trying to understand the processes that originated such a huge diversity of parasites [3], and how such diversity determines the evolution of hosts' resistance mechanisms.

The group

Research on blood parasites is being carried out in the frame of a collaboration among several people from different institutions. My main collaborator is Staffan Bensch, at the Molecular Population Biology Laboratory in Lund University (Sweden). I'm collaborating with Staffan's team in a broad-scale study on the ecology and evolution of malaria parasites. I'm also participating in a project on the implications of introduced malaria parasites in New Zealand, in collaboration with John Ewen (Institute of Zoology, Zoological Society of London, UK) and Camille Bonneaud (Department of Organismic and Evolutionary Biology, Harvard University, USA). I'm also collaborating with David S. Richardson (University of East Anglia, Norwich, UK) in a research line on phenotypic variation and population genetics of birds in Atlantic archipelagos, with special reference to the evolution of parasite resistance. This connection has been recently reinforced with the stay of Álvaro Ramírez as a postdoc in the laboratory in Norwich.

References

1. Pérez-Tris, J., Hasselquist, D., Hellgren, O., Krizanauskiene, A., Waldenström, J. & Bensch, S. 2005. What are malaria parasites? Trends in Parasitology 21: 209-211. [PDF]

2. Bensch, S., Pérez-Tris, J., Waldenström, J. & Hellgren, O. 2004. Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: multiple cases of cryptic speciation? Evolution 58: 1617-1621. [PDF]

3. Pérez-Tris, J., Hellgren, O., Križanauskienė, A., Waldenström, J., Secondi, J., Bonneaud, C., Fjeldså, J., Hasselquist, D. & Bensch, S. 2007. Within-host speciation of malaria parasites. PLoS ONE 2: e235. [Open access]

4. Reullier, J., Pérez-Tris, J., Bensch, S. & Secondi, J. 2006. Diversity, distribution and exchange of blood parasites meeting at an avian moving contact zone. Molecular Ecology 15: 753-763. [PDF]

5. Pérez-Tris, J. & Bensch, S. 2005. Dispersal increases local transmission of avian malarial parasites. Ecology Letters 8: 838-845. [PDF]

6. Bonneaud, C., Pérez-Tris, J., Federici, P., Chastel, O. & Sorci, G. 2006. Major histocompatibility alleles associated with local resistance to malaria in a passerine. Evolution 60: 383-389. [PDF]