Evolution of host specificity in fleas: Is it directional and irreversible? Robert Poulin a, * , Boris R. Krasnov b , Georgy I. Shenbrot b , David Mouillot c , Irina S. Khokhlova d a Department of Zoology, University of Otago, P.O. Box 56, Dunedin, New Zealand b Ramon Science Center and Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, P.O.Box 194, Mizpe Ramon 80600, Israel c UMR CNRS-UMII 5119 Ecosystemes Lagunaires, University of Montpellier II, CC093, FR-34095 Montpellier Cedex 5, France d Desert Animal Adaptations and Husbandry, Wyler Department of Dryland Agriculture, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede Boqer Campus, 84990, Israel Received 21 July 2005; received in revised form 25 September 2005; accepted 30 September 2005 Abstract Evolutionary trends in the evolution of host specificity have been the focus of much discussion but little rigorous empirical testing. On the one hand, specialization is often presumed to lead irreversibly into evolutionary dead ends and little diversification; this would mean that generalists might evolve into specialists, but not vice versa. On the other hand, low host specificity may limit the risk of extinction and provide more immediate fitness benefits to parasites, such that selection may favour evolution toward a generalist strategy. Here, we test for directionality in the evolution of host specificity using a large data set and phylogenetic information on 297 species of fleas parasitic on small mammals. The analyses determined whether host specificity, measured both as the number of host species exploited and their taxonomic diversity, was related to clade rank of the flea species, or the number of branching events between an extant species and the root of the phylogenetic tree (i.e., the total path length from the root of the tree to the species). Based on regression analyses, we found positive relationships between the number of host species used and clade rank across all 297 species, as well as within one (Hystrichopsyllidae) of four large families and one of seven large genera investigated separately; in addition, we found a positive relationship between the taxonomic diversity of host species used and clade rank in another of the seven genera. These results suggest a slight evolutionary trend of decreasing host specificity. Using a much more conservative likelihood ratio test, however, a random walk, or null model, of evolution could not be discarded in favour of the directional trends in all cases mentioned above. Still, these results suggest that host specificity may have tended to decrease in many flea lineages, a process that could have been driven by the benefits of exploiting a wide range of host species. q 2005 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved. Keywords: Clade rank; Likelihood ratio test; Phylogeny; Random walk; Siphonaptera 1. Introduction In evolutionary biology, specialization is generally pre- sumed to be irreversible. Mayr (1963) has famously argued that specialization leads into blind alleys, and that highly specialized organisms do not give rise to new lineages. This notion is usually applied to morphological specialization, as when Noble and Noble (1976) stated that parasites, with their reduced morphological complexity well-fitted to their mode of life, were good examples of evolution’s inexorable march into dead ends. Specialization can also be viewed from an ecological perspective and measured as the diversity of resources used by an organism (Futuyma and Moreno, 1988). On the one hand, specialist taxa, capable of using only a narrow range of resources, should be less likely to colonize new habitats and therefore the potential of specialists to give rise to new lineages should be limited (Jaenike, 1990). If this is so, we might expect that generalists can evolve into specialists but that the likelihood of specialists evolving into generalists would be much lower. Thus, within a clade, the more specialized species should, on an average, be the more derived, i.e. the more recent ones. On the other hand, specialist taxa should be more prone to extinction than generalists, because of their strict dependence on a narrow resource base and thus we might expect generalist taxa to be favoured and to proliferate over evolutionary time. International Journal for Parasitology 36 (2006) 185–191 www.elsevier.com/locate/ijpara 0020-7519/$30.00 q 2005 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.ijpara.2005.09.017 * Corresponding author. Tel.: C64 3 479 7983; fax: C64 3 479 7584. E-mail address: robert.poulin@stonebow.otago.ac.nz (R. Poulin).