taxonomy.zoology.gla.ac.u
Roderic D. M. Page, Patricia L. M. Lee, S. Anette Becher,
Richard Griffiths, and Dale H. Clayton
Related Web links
Tree of Life louse pages
TreeMap software
Dennyus Scanning electron micrographs
Host-Parasite Cospeciation
A key question in the study of coevolution is the tempo and mode of evolution of the interacting partners. Is the association an ancient one, reflecting a long and intimate interaction between the two organisms, or is it a recent event due perhaps to a parasite colonising a new host?
What is the relative rate of evolution between host and parasite? Answering these questions requires the comparison of evolutionary trees (phylogenies) for host and parasite (Figure 1). To the extent that the trees match, host and parasite have cospeciated, that is, parasite and host speciated at the same time. Mismatches between the host and parasite phylogenies signal processes other than cospeciation, such as host switching, speciation by parasites independently of their hosts, and parasite extinction (Page, Clayton et al. 1996). Because cospeciating taxa are, by definition, contemporaneous, we can compare amounts of evolutionary divergence in cospeciating pairs of hosts and parasites to measure relative rates of evolution in the two clades. Because host and parasite are often taxonomically distant (e.g., birds and insects), with differing generation times, population sizes, and metabolic rates, they are ideal systems to investigate the influence of these factors on rates of evolution Swiftlets and lice
The two dozen species of swiftlets and their lice show great promise as a model system for studying cospeciation. The lice are host specific, and transmission of Dennyus lice between individual hosts is known to be strictly vertical (between parent bird and its offspring) (Lee and Clayton 1995), suggesting that opportunities for colonizing new host taxa are quite limited. Swiftlets predominantly nest in caves (Figure 2), often in large colonies. This makes it feasible to undertake transfer experiments to test the survival of lice moved to foreign hosts.
Why use molecular data?
Swiftlet species are often difficult to distinguish morphologically (Figure 3), indeed the best guide to the identity of an individual is often its nest. Swiftlet nest structure is useful taxonomically, but is not phylogenetically informative
Dennyus lice show limited morphological variation, and some taxa were only discovered by using multivariate morphometrics. This morphological conservatism prevents cladistic analysis, so the only morphological estimate of relationships available is a cluster analysis of morphometric data While molecular data are useful in cases like this where morphological data is limited, there are two other compelling reasons to use DNA sequences in studies of host-parasite cospeciation:
• Homologous characters can be obtained for both hosts and parasites. In such taxonomically disparate taxa as birds and insects there are few homologous morphological characters which can be compared, whereas there are many genes that are homologous. Furthermore, molecular data permit the use of the same units (e.g., numbers of nucleotide substitutions per site) to measure evolutionary change, which is essential if we wish to compare rates of evolution.
• Molecular information can provide data on the relative ages of the host and parasite clades. Information on lineage age can help distinguish between host switching and the persistence of relict parasite lineages as alternative explanations of incongruence between host and parasite phylogenies.
Data and Analysis
DNA sequences for an homologous region of the mitochondrial (mtDNA) cytochrome b gene were obtained from swiftlets and their lice using standard techniques (Lee, Clayton et al. 1996; Page, Lee et al. submitted). Dennyus lice feed on both feathers and blood, so to minimise the chances of mistaking host DNA for louse DNA the lice were starved for 24 hours prior to death. Sequences obtained from the insects were different from any bird sequence we obtained, and readily aligned with other insects (Figure 6). Different tree building methods yielded similar trees, differing only in resolving relationships among some distinctus species-group lice for which the phylogenetic signal is fairly weak. Conformity to molecular clocks was tested using maximum likelihood tests. Host and parasite trees were compared using TREEMAP (Page 1994). For contrasting views on the most appropriate of comparing host and parasite trees see Hoberg et al. (1997) and Paterson and Gray (1997).
Have swiftlets and lice cospeciated?
Detailed reconstruction of the history of a host-parasite association requires robust, fully resolved trees. Because of some areas of uncertainty in the louse phylogeny we can confidently compare only part of the trees
Louse mtDNA is rapidly evolving
Although Dennyus lice are very morphologically conservative, their mitochondrial DNA is highly divergent. The distinctus and thompsoni species groups differ only in minor details of head shape and setation (Figure 4), and yet show 25-30% DNA sequence divergence – greater than the divergence between swifts and and their sister taxon the Comparisons of cytochrome b amino acid sequences between lice and other insects (honeybee, fruitfly, mosquito and locust) show that Dennyus is among the most divergent insects known (Figure 8). This variation in rate of insect mtDNA evolution means that calibrations of absolute rate of evolution in other insects (for example, that based on the age of Hawiaiin island Drosophila) will not apply to lice, hence it is difficult to independently estimate the age of the lice relative to their hosts. However, we can directly compare amounts of sequence divergence in birds and lice.
Lice evolve more rapidly than their hostshummingbirds.
