A hitchhikers guide to the Galápagos: co-phylogeography of Galápagos mockingbirds and their parasites

Background: Parasites are evolutionary hitchhikers whose phylogenies often track the evolutionary history of their hosts. Incongruence in the evolutionary history of closely associated lineages can be explained through a variety of possible events including host switching and host independent speciation. However, in recently diverged lineages stochastic population processes, such as retention of ancestral polymorphism or secondary contact, can also explain discordant genealogies, even in fully co-speciating taxa. The relatively simple biogeographic arrangement of the Galapagos archipelago, compared with mainland biomes, provides a framework to identify stochastic and evolutionary informative components of genealogic data in these recently diverged organisms. Results: Mitochondrial DNA sequences were obtained for four species of Galapagos mockingbirds and three sympatric species of ectoparasites - two louse and one mite species. These data were complemented with nuclear EF1 alpha sequences in selected samples of parasites and with information from microsatellite loci in the mockingbirds. Mitochondrial sequence data revealed differences in population genetic diversity between all taxa and varying degrees of topological congruence between host and parasite lineages. A very low level of genetic variability and lack of congruence was found in one of the louse parasites, which was excluded from subsequent joint analysis of mitochondrial data. The reconciled multi-species tree obtained from the analysis is congruent with both the nuclear data and the geological history of the islands. Conclusions: The gene genealogies of Galapagos mockingbirds and two of their ectoparasites show strong phylogeographic correlations, with instances of incongruence mostly explained by ancestral genetic polymorphism. A third parasite genealogy shows low levels of genetic diversity and little evidence of co-phylogeny with their hosts. These differences can mostly be explained by variation in life-history characteristics, primarily host specificity and dispersal capabilities. We show that pooling genetic data from organisms living in close ecological association reveals a more accurate phylogeographic history for these taxa. Our results have implications for the conservation and taxonomy of Galapagos mockingbirds and their parasites

Discordant population histories of host and its parasite: A role for ecological permeability of extreme environment?

Biogeographical and ecological barriers strongly affect the course of micro-evolutionary processes in free living organisms. Here we assess the impact of a recently emerged barrier on populations of limnic fauna. Genetic diversity and population structure in a host-parasite system (Wenyonia virilis tapeworm, Synodontis schall catfish) are analyzed in the recently divided Turkana and Nile basins. The two basins, were repeatedly connected during the Holocene wet/dry climatic oscillations, following late Pleistocene dessication of the Turkana basin. Mitochondrial DNA sequences for cytochrome oxidase I gene (cox I) and a whole genome scanning method-amplified fragment length polymorphism (AFLP) were employed. A total of 347 cox I sequences (representing 209 haplotypes) and 716 AFLP fragments, as well as 120 cox I sequences (20 haplotypes) and 532 AFLP fragments were obtained from parasites and hosts, respectively. Although results indicate that host and parasite populations share some formative traits (bottlenecks, Nilotic origin), their population histories/patterns differ markedly. Mitochondrial analysis revealed that parasite populations evolve significantly faster and show remarkably higher genetic variability. Analyses of both markers confirmed that the parasites undergo lineage fission, forming new clusters specific for either freshwater or saline parts of Lake Turkana. In congruence with the geological history, these clusters apparently indicate multiple colonisations of Lake Turkana from the Nile. In contrast, the host population pattern indicates fusion of different colonisation waves. Although fish host populations remain connected, saline habitats in Lake Turkana (absent in the Nile), apparently pose a barrier to the gene flow in the parasite, possibly due to its multihost lifecycle, which involves freshwater annelids. Despite partially corroborating mitochondrial results, AFLP data was not sufficiently informative for analyzing populations with recently mixed biogeographic histories

Substitution models for nucleotide data partitions of the <i>Wenyonia</i> spp. coxI dataset selected using the AIC in PartitionFinder for BI and ML runs.

<p>Substitution models for nucleotide data partitions of the <i>Wenyonia</i> spp. coxI dataset selected using the AIC in PartitionFinder for BI and ML runs.</p

Results of population genetic statistics of mtDNA for both parasites and hosts.

<p>Results of population genetic statistics of mtDNA for both parasites and hosts.</p

Sampling localities, coordinates and sample sizes.

<p>Sampling localities, coordinates and sample sizes.</p

Individual-based cluster representation of all sampled <i>Wenyonia</i> spp. (a) and <i>Synodontis</i> spp. (b) as revealed by the Bayesian inference of population structure.

<p>Each colour represents one assumed population cluster K. Multiple coloured bars display an individual’s estimated membership proportion in more than one population (q), i.e. admixture. Turkana—medium 1–3 refers to three different localities: 1, Central Island; 2, Kerio River delta; 3, Kalokol.</p