Host-parasite cospeciation: An annotated bibliography

C.J. Clark

Theoretical Ecology

Baker, M. D., Vossbrinck, C. R., Becnel, J. J. & Andreadis, T. G. 1998. Phylogeny of Amblyospora (Microsporida: Amblyosporidae) and related genera based on small subunit ribosomal DNA data: A possible example of host parasite cospeciation. Journal of Invertebrate Pathology 71, 199-206. The authors analyzed gene sequences for six species of microsporidia from mosquito hosts using parsimony, maximum likelihood, and distance methods. They identified identical trees and suggested that the focal microsporidian taxa form a monophyletic group. They conclude that the pattern of host relationships on the tree provides preliminary evidence that host-parasite cospeciation is an important mechanism of evolution in this group.

Brooks, D.R. 1979. Testing the context and extent of host-parasite coevolution. Systematic Zoology, 28, 299-307. This paper provided the first discussion of the systematic perspective of cospeciation using phylogenetics. The author used the term co-evolution to include systematic and ecological perspectives, then characterized each view separately as a subset of co-evolution (term co-evolution first introduced by Ehrlich and Raven 1964). Cospeciation- The systematic view. Stressed the degree of congruence and incongruence between host and parasite phylogenies. Co-accommodation or co-adaptation - The ecological view. Stressed the ways in which host and parasites, or insects and plants, interact and survive together. Brooks used host specificity as a focus of discussion to show that patterns of co-adaptation did not necessarily predict cospeciation patterns. He argued that robust explanations of co-evolution had to incorporate elements of both within a phylogenetic framework.

Carreno, R. A. & Hoberg, E. P. 1999. Evolutionary relationships among the protostrongylidae (Nematoda: Metastrongyloidea) as inferred from morphological characters, with consideration of parasite-host coevolution. Journal of Parasitology 85, 638-648. This paper reconstructs the phylogeny of representative species of the apicomplexan (Haemosporina) using morphological characters. Supposed patterns of parasite-host coevolution are then elucidated by examining host-distribution relative to the phylogeny of their parasites. The authors conclude there was no pattern of strict cospeciation between parasites and their host groups. However, they suggest there is stronger evidence of coevolution of parasites with their vectors than with their vertebrate hosts.

Charleston, M. A. 1998. Jungles: A new solution to the host/parasite phylogeny reconciliation problem. Mathematical Biosciences 149, 191-223. Frankly, I didn’t quite get this paper. It provides a method of listing all of the optimal solutions to finding “least cost” reconstructions of host-parasite associations given their phylogenetic histories. The author considers each hypothesized past association individually, in a structure termed a “Jungle”. Charleston explains how these structures enable fast “acquisition of globally optimal solutions” using weighting schemes, including minimization of total number of postulated events and maximization of postulated cospeciation events. He uses the pocket gopher/chewing louse system investigated by Hafner and Nadler as an example.

Dabert, J. & Mironov, S. V. 1999. Origin and evolution of feather mites (Astigmata). Experimental and Applied Acarology 23, 437-454. This paper presents general information about feather mites’ morphological adaptations, evolutionary strategies and phlogenetic relationships. It also offers examples of host-parasite cospeciation and hypotheses on the evolution of morphological adaptations of feather mites during colonization and establishment in different microhabitats. The authors construct a general feather mite phylogeny for the Analgoidea superfamily. They postulate cospeciation of parasites with their hosts as a main factor driving feather mite evolution, though they offer no rigorous analysis to support this.

Demastes, J. W. & Hafner, M. S. 1993 Cospeciation of pocket gophers (Geomys) and their chewing lice (Geomydoecus). Journal of Mammalogy 74, 521-530. This paper compares phylogenies for pocket gophers and their chewing lice. Their results suggest a history of widespread cospeciation in this host-parasite assemblage. Cospeciation was strongly supported with statistical comparison of genetic-distance matrices for gophers and lice. Host and parasite phylogenies were not identical however. The authors suggest incongruence likely results from host-switching by the parasites, retention of ancestral taxa of parasites on recently evolved hosts, or poorly delineated taxonomic boundaries.

Eichler, W. 1941. Wirstsspezifitat und stammesgeschichtliche Gleichlaufigkeit bei Parasiten allgemeinen und bei Mallophagen im besonderen. Zoologische Anzeiger, 132, 254-62. Took Fahernholz's concept and refined it to say that cospeciation was accepted as the only mechanism involved in parasite evolution. Parasite taxonomy was equated with host taxonomy (phylogeny) and absolute specificity was required by definition. He negated the possibility of host switching as an influence on diversification.

Farhenholz, H. 1913. Ectoparasiten und Abstammungslehre. Zoologische Anzeiger, 41, 371-374. Also studied avian lice. Argued that parasites speciated in response to differences in their hosts, and considered specificity of paramount importance in cospeciation.

Haag, J., O'Huigin, C. & Overath, P. 1998. The molecular phylogeny of trypanosomes: Evidence for an early divergence of the Salivaria. Molecular and Biochemical Parasitology 91, 37-49. The authors present a molecular phylogenetic reconstruction of trypanosome evolution. The branching order of the non-Salivarian trypanosomes supports host-parasite cospeciation scenarios, but also suggests host switches, e.g. between bird and reptilian trypanosomes.

Hafner, M. S., Sudman, P. D., Villablanca, F. X., Spradling, T. A., Demastes, J. W. & Nadler, S. A. 1994. Disparate rates of molecular evolution in cospeciating hosts and parasites. Science (Washington D C) 265, 1087-1090. Using DNA sequences for pocket gophers and their chewing lice, the authors provide evidence for cospeciation and reveal different rates of molecular evolution in the hosts and their parasites. They found the rate of nucleotide substitution is three times higher in lice than their hosts, and that the rate of synonymous substitution was an order of magnitude greater in lice. They suggest the difference in synonymous substitution rate between lice and gophers correlates with a difference in generation times. Data presented here has been used over and over again for re-examination with new more sophisticated models.

Hafner, M. S. & Page, R. D. M. 1995. Molecular phylogenies and host-parasite cospeciation: Gophers and lice as a model system. Philosophical Transactions of the Royal Society of London B Biological Sciences 349, 77-83. The authors again use the example of pocket gophers and their lice to illustrate that a variety of questions that can be addressed through phylogenetic study of host-parasite systems. They describe how comparisons of phylogenetic trees for hosts and their parasites can determine the extent to which groups have cospeciated. They suggest that features compared in the hosts and parasites should be genetically based, evolutionarily homologous, and should evolve in a roughly time-dependent fashion within each group and advocate nucleotide sequences encoding homologous genes in hosts and parasites for comparative studies of evolutionary rates.

Hoberg, E. P., Brooks, D. R. & Siegel-Causey, D. 1997. Host-parasite cospeciation: History, principles, and prospects, pp. 212-235. The authors address host-parasite cospeciation and review the history of research on cospeciation and the methods for comparing host-parasite phylogenies. They emphasize Brooks parsimony analysis and bird-helminth systems. Though the authors find problems with both Brooks parsimony and component analysis in detecting host-parasite cospeciation, they weakly argue that Brooks parsimony is the better approach as it allows host-switching events, not allowed in components analysis. Note: Later component analysis (Page 1998) suggests that host-switching can be incorporated into component analysis.

Hoberg, E. P., Jones, A., Rausch, R. L., Eom, K. S. & Gardner, S. L. 2000. A phylogenetic hypothesis for species of the genus Taenia (Eucestoda: Taeniidae). Journal of Parasitology. 86, 89-98. Hoberg et al. use cladistic analysis of a numerical data matrix describing 27 characters for species of Taenia. This resulted in 4 most parsimonious phylogenetic trees. The authors suggest that cospeciation with respect to carnivorous definitive hosts and Taenia is limited and that current associations result from extensive host-switching among felids, canids, and hyaenids. However, parasite relationships with herbivorous intermediate hosts suggest coevolution.

Hugot, J.-P. 1998. Phylogeny of neotropical monkeys: The interplay of morphological molecular, and parasitological data. Molecular Phylogenetics and Evolution 9, 408-413. In this paper the results of a morphologically based cladistic analysis of pinworms of the Platyrrhini is used as an estimate of the phylogeny of certain primates. The parasite-treewas combined, using parsimony analysis, with several conflicting molecular or morphological hypothesis of the phylogeny of the host group. The authors rather weakly interpret their results as evidence for close coevolution between the Platyrrhini and their specific pinworms.

Kellogg, V.L. 1896a. New Mallophaga, I- with special reference to a collection made form maritime birds of the Bay of Monterey, California. Proceedings of the California Academy of Sciences, 6, 31-196. Kellogg worked on the lice of birds, and noted that host specificity could be great in these systems. He also recognized that some species were not host specific. Lack of host specificity was attributed to dual causes: (1) Host switching between or among ecologically similar birds (straggling); (2) the same parasite occurring on multiple host species that were geographically isolated (inferring persistence of a parasite on phylogenetically related avian species that had shared a common ancestor).

Kellogg, V.L. 1913. Distribution and species forming of ectoparasites. American Naturalist, 47, 129-58. In this paper Kellogg expanded his original work and predicted that phylogenetic relatedness, rather than ecological interactions and adaptations, provide the basis for explaining host specificity and speciation. He identified cospeciation as a major determinant of structure in host-parasite assemblages, but also recognized the possibility of more complex interactions involving host switching.

Klassen, G.J. 1992. Coevolution: a history of the macroevolutioary approach to studying host-parasite associations. Journal of Parasitology, 78, 573-87. Klassen offers an excellent description of the history of the study of host-parasite associations and descirbes a series of rules which he calls the co-evolutionary paradigm that has dominated the field for nearly a century: Fahernholz’s rule- Parasite phylogeny mirrors host phylogeny; Szidat’s rule – The more primitive the host, the more primitive the parasites which it harbors; Eichler’s rule- diverse host groups will harbor greater numbers of parasites than less diverse host taxa; Manter’s rules- (a) Parasites evolve more slowly than their hosts, and (b) the longer the association within a particular host group, the greater the specificity exhibited by the parasite; Fuhrmann’s rule – Each avian order has its own group of specific cestodes.

Manter, H.W. 1940. The geographical distribution of digenetic trematodes of marine fishes of the tropical American Pacific. Allan Hancock Pacific Expedition Reports, 2, 531-47. Manter expanded concepts developed by Kellogg to recognize that the degree of host specificity appeared to vary in direct correlation with the taxonomic rank at which host-parasite cospeciation was observed. He proposed that parasite speciation lagged behind that of the host group and linked the degree of specificity to the temporal duration of an association.

Mironov, S. V. & Dabert, J. 1999. Phylogeny and cospeciation in feather mites of the subfamily Avenzoariinae (Analgoidea: Avenzoariidae). Experimental and Applied Acarology 23, 525-549. This paper uses cladistic analysis of phylogenetic relationships for the feather mite subfamily Avenzoariinae. A comparative analysis of phylogenetic hypotheses for the subfamily indicates cospeciation of feather mites with their hosts. The authors claim that the expected pattern of evolution was disturbed by different evolutionary events, such as host shifts, extinction of mites and differential evolutionary rates of mite lineages in different phyletic branches of feather parasites.

Page, R. D. M. 1993. Parasites, phylogeny and cospeciation. International Journal for Parasitology 23, 499-506. This paper describes then recent contributions to the field of host-parasite association, and shows how phylogenies can be used to explore many questions regarding origins of specific host-parasite relationships. Page reviews many aspects of phylogeny that are relevant to the comparison of host and parasite phylogenies and discusses some of the problems of comparing host and parasite trees. Specifically, he focuses on the difficulties in interpreting incongruence between trees.

Page, R.D.M. 1994. Parallel phylogenies: reconstructing the history of host-parasite assemblages. This paper describes a method for reconstructing the history of a host-parasite assemblage. The paper was motivated by inadequate methods for comparing host and parasite phylogenies, namely the unsatisfactory choice between one method (Brooks parsimony analysis) that incorporates host transfer but can lead to internal inconsistencies, and another method (reconciled trees) that discounts host-switching altogether. The author proposes a method for reconciling two trees to include host switching, and develops a criterion for choosing among possible reconstructions of host-parasite evolution. The author shows reconstructions that maximize the number of speciation events in the parasite phylogeny that can be attributed to cospeciation with their hosts are preferred over reconstructions that postulate fewer cospeciations.

Page, R. D. M. 1994. Maps between trees and cladistic analysis of historical associations among genes, organisms, and areas. Systematic Biology 43, 58-77. In this paper, Page discusses the use of reconciled trees on studies of hot-parasite coevolution. He also describes an algorithm for their computation, and develops measures to quantify the degree of fit between host and associated tress. Finally, he introduces the concept of maximizing the amount of codivergence between the associates as a means of addressing the problem of horizontal transmission of parasites.

Page, R. D. M. 1996. Temporal congruence revisited: Comparison of mitochondrial DNA sequence divergence in cospeciating pocket gophers and their chewing lice. Systematic Biology 45, 151-167. Here, Page uses molecular techniques to establish phylogenetic trees and describes methods for comparing sequence divergence in hosts and parasites. These methods are (surprise, surprise) applied to data for pocket gophers and their chewing lice. The hypothesis of cospeciation between these two clades is strongly supported. The lengths of homologous branches in the gopher and louse phylogenies are positively correlated, but there is little support for the hypothesis that lice are evolving an order of magnitude faster than are their hosts.

Page, R. D. M. and Hafner, M. S. 1996. Molecular phylogenies and host-parasite cospeciation: Gophers and lice as a model system. In New usesfor new phylogenies. Harvey, P.H., Brown A.J., Smith J.M, and Nee, S eds. Oxford University Press, New York, NY. This is the paper we read for class. Page and Hafner introduce a three-step protocol for investigations of cospeciation: tree building, tree comparison, and estimation of divergence. They AGAIN use the example of pocket gophers and their lice. The authors emphasize the importance of using molecular divergence to test reconstructions of host and parasite phylogenies and to calculate time of divergence of cospeciating clades. Though both molecular and mathematical approaches to studying host-parasite cospeciation have greatly improved. Few researchers have utilized these tools, and the authors strongly encourage further research in this area.

Page, R. D. M., Lee, P. L. M., Becher, S. A., Griffiths, R. & Clayton, D. H. 1998. A different tempo of mitochondrial DNA evolution in birds and their parasitic lice. Molecular Phylogenetics and Evolution 9, 276-293. In this paper, Page et al. construct a phylogeny for the lice on swiftlets (no gophers?) based on mitochondrial cytochrome b DNA sequences. Comparison with a previously obtained phylogeny for the hosts indicates some degree of cospeciation. Cospeciation events were used to compare relative rates of evolution in the birds and their lice. Louse were found to be evolving two to three times more rapidly in than their hosts. Disparity in evolutionary rates were explained by the small effective population sizes of lice coupled with founder events occurring during transmission to new host.

Paterson, A.M, Gray, R.D, and Wallis, G.P. 1993. Parasites, petrels and penguins: does louse presence reflect seabird phylogeny? This study investigates the host-parasite relationships of seabirds and their chewing lice for evidence of cospeciation. The authors used cladistic methods and component analysis to investigate whether the presence or absence of lice genera reflects the phylogeny of seabird taxa. Trees were more similar to the independent host phylogeny than would be expected due to chance. The authors conclude that the louse presence or absence on seabirds contain information on bird phylogeny, indicating that cospeciation has occurred. They suggest that much of the radiation of lice genera pre-dated the radiation of seabirds. This is one of the few papers that actually uses the steps deemed necessary by Page to determine cospeciation.

Paterson, A. M. & Gray, R. D. 1997. Host-parasite cospeciation, host switching, and missing the boat, pp. 236-250. The authors address host-parasite cospeciation and contrast the method of component analysis with Brooks Parsimony Analysis, which they apply to bird-ectoparasite systems. The authors conclude that component analysis is the better method for detecting cospeciation event.

Paterson, A. M. & Poulin, R. 1999. Have chondracanthid copepods co-speciated with their teleost hosts? Systematic Parasitology 44, 79-85. This paper examined copepods from the genus Chondracanthus and their teleost hosts for evidence of a close co-evolutionary association by comparing host and parasite phylogenies using TreeMap analysis. In general, significant cospeciation was observed and instances of host switching were rare.

Paterson, A. M., Palma, R. L. & Gray, R. D. 1999. How frequently do avian lice miss the boat? Implications for coevolutionary studies. Systematic Biology 48, 214-223. These authors examine different methods for analyzing host-parasite cospeciation (Brooks parsimony analysis and reconciliation analysis) and argue that, because these methods can produce quite different results, increased attention should be paid to the biological likelihood of different types of coevolutionary events (such as extinction, sampling error, and missing the boat) when choosing a method for coevolutionary analysis. The authors test the idea that missing the boat has been an important factor in bird-louse coevolutionary history by examining bird-louse distributions where they could clearly identify a parent-daughter relationship between bird taxa. Their result imply that sorting events, probably from parasites missing the boat, are extremely common in the coevolutionary history of birds and lice.

Ronquist, F. 1995. Reconstructing the history of host-parasite associations using generalized parsimony. Cladistics 11, 73-89. This paper is largely a criticism of methods of reconstructing the history of host-parasite associations that do not consider processes, such as cospeciation and host switching, that may affect an association. The author provides a method that distinguishes between host tracking and host switching. He converts the host phylogeny into a cost matrix, allowing for host switching, and uses generalized-parsimony algorithms to find minimum-cost reconstructions of the history of the host-parasite association. The author applies this method by re-examining the Hafner pocket gopher/chewing lice data.

Rozsa, L. 1993. Speciation patterns of ectoparasites and "straggling" lice. International Journal for Parasitology 23, 859-864. This paper offers a short history of host-parasite coevolution studies, focusing on two competing views that explain ectoparasite speciation patterns, one emphasizing cospeciation and one emphasizing host-switching. The author holds that available phylogenetic trees cannot be interpreted without revisiting island biogeography theory, explaining that parasite extinction due to a temporal decline in host population size seems to be a prerequisite of subsequent speciation by host-switch. The paper was not exactly data rich. The author concludes the paper by emphasizing the need for a re-evaluation of "stragglers" (ectoparasites found on non-specific hosts) in host-parasite cospeciation studies.