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A parasite reveals cryptic phylogeographic history of its host.

ABSTRACT: This study compares the continental phylogeographic patterns of two wild European species linked by a host-parasite relationship: the field mouse Apodemus sylvaticus and one of its specific parasites, the nematode Heligmosomoides polygyrus. A total of 740 base pairs (bp) of the mitochondrial cytochrome b (cyt b) gene were sequenced in 122 specimens of H. polygyrus and compared with 94 cyt b gene sequences (974 bp) previously acquired for A. sylvaticus. The results reveal partial spatial and temporal congruences in the differentiation of both species' lineages: the parasite and its host present three similar genetic and geographical lineages, i.e. Western European, Italian and Sicilian, and both species recolonized northwestern Europe from the Iberian refuge at the end of the Pleistocene. However, H. polygyrus presents three particular differentiation events. The relative rate of molecular evolution of the cyt b gene was estimated to be 1.5-fold higher in the parasite than in its host. Therefore, the use of H. polygyrus as a biological magnifying glass is discussed as this parasite may highlight previously undetected historical events of its host. The results show how incorporating phylogeographic information of an obligate associate can help to better understand the phylogeographic pattern of its host.

SUBMITTER: Nieberding C

PROVIDER: S-EPMC1691906 | biostudies-other | 2004 Dec

REPOSITORIES: biostudies-other

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A parasite reveals cryptic phylogeographic history of its host.

Nieberding C C Morand S S Libois R R Michaux J R JR

Proceedings. Biological sciences 20041201 1557

This study compares the continental phylogeographic patterns of two wild European species linked by a host-parasite relationship: the field mouse Apodemus sylvaticus and one of its specific parasites, the nematode Heligmosomoides polygyrus. A total of 740 base pairs (bp) of the mitochondrial cytochrome b (cyt b) gene were sequenced in 122 specimens of H. polygyrus and compared with 94 cyt b gene sequences (974 bp) previously acquired for A. sylvaticus. The results reveal partial spatial and temp ...[more]

PMID: 15615681

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Project description:There is growing interest in the role that life-history traits of hosts, such as their 'pace-of-life', play in the evolution of resistance and tolerance to parasites. Theory suggests that, relative to host species that have high syntopy (local spatial and temporal overlap) with parasites, host species with low syntopy should have lower selection pressures for more constitutive (always present) and costly defences, such as tolerance, and greater reliance on more inducible and cheaper defences, such as behaviour. Consequently, we postulated that the degree of host-parasite syntopy, which is negatively correlated with host pace-of-life (an axis reflecting the developmental rate of tadpoles and the inverse of their size at metamorphosis) in our tadpole-parasitic cercarial (trematode) system, would be a negative and positive predictor of behavioural resistance and tolerance, respectively. To test these hypotheses, we exposed seven tadpole species to a range of parasite (cercarial) doses crossed with anaesthesia treatments that controlled for anti-parasite behaviour. We quantified host behaviour, successful and unsuccessful infections, and each species' reaction norm for behavioural resistance and tolerance, defined as the slope between cercarial exposure (or attempted infections) and anti-cercarial behaviours and mass change, respectively. Hence, tolerance is capturing any cost of parasite exposure. As hypothesized, tadpole pace-of-life was a significant positive predictor of behavioural resistance and negative predictor of tolerance, a result that is consistent with a trade-off between behavioural resistance and tolerance across species that warrants further investigation. Moreover, these results were robust to considerations of phylogeny, all possible re-orderings of the three fastest or slowest paced species, and various measurements of tolerance. These results suggest that host pace-of-life and host-parasite syntopy are powerful drivers of both the strength and type of host defence strategies against parasites. Future research should evaluate how often and how strongly host pace-of-life and host-parasite syntopy are correlated and which is the better predictor of the strength and type of host investments in anti-parasite defences.

Project description:BACKGROUND:Coalescent methods that use multi-locus sequence data are powerful tools for identifying putatively reproductively isolated lineages, though this approach has rarely been used for the study of microbial groups that are likely to harbor many unrecognized species. Among microbial symbionts, integrating genetic species delimitation methods with trait data that could indicate reproductive isolation, such as host specificity data, has rarely been used despite its potential to inform species limits. Here we test the ability of an integrative approach combining genetic and host specificity data to delimit species within the avian malaria parasite genus Leucocytozoon in central Alaska. RESULTS:We sequenced seven nuclear loci for 69 Leucocytozoon samples and used multiple species delimitation methods (GMYC and BPP models), tested for differences in host infection patterns among putative species based on 406 individual infections, and characterized parasite morphology. We found that cryptic morphology has masked a highly diverse Leucocytozoon assemblage, with most species delimitation methods recovering support for at least 21 separate species that occur sympatrically and have divergent host infection patterns. Reproductive isolation among putative species appears to have evolved despite low mtDNA divergence, and in one instance two Leucocytozoon cytb haplotypes that differed by a single base pair (~?0.2% divergence) were supported as separate species. However, there was no consistent association between mtDNA divergence and species limits. Among cytb haplotypes that differed by one to three base pairs we observed idiosyncratic patterns of nuclear and ecological divergence, with cytb haplotype pairs found to be either conspecific, reproductively isolated with no divergence in host specificity, or reproductively isolated with divergent patterns of host specialization. CONCLUSION:Integrating multi-locus genetic species delimitation methods and non-traditional ecological data types such as host specificity provide a novel view of the diversity of avian malaria parasites that has been missed previously using morphology and mtDNA barcodes. Species delimitation methods show that Leucocytozoon is highly species-rich in Alaska, and the genus is likely to harbor extraordinary species-level diversity worldwide. Integrating genetic and ecological data will be an important approach for understanding the diversity and evolutionary history of microbial symbionts moving forward.

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A parasite reveals cryptic phylogeographic history of its host.

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A parasite reveals cryptic phylogeographic history of its host.

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