Evolution of host specificity in fleas: Is it directional and irreversible?

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.

Introduction

In evolutionary biology, specialization is generally presumed 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. It is therefore not straightforward to predict in which direction specialization will evolve in a given clade, i.e. whether it will tend to increase or decrease over evolutionary time. Indeed, based on a review of the limited evidence available from a range of ecological systems, Thompson (1994) has concluded that there is no intrinsic direction to the evolution of ecological specialization.

Directionality and irreversibility in the evolution of ecological specialization are not easy to test, mainly because defining resource breadth for many different taxa is often problematic. Using parasitic organisms can provide a solution to this obstacle (Adamson and Caira, 1994). For parasites, ecological specialization can be defined in terms of host specificity, i.e. the number and diversity of host species used by a parasite. In a recent study, for instance, Desdevises et al. (2002) have mapped the host specificity of 20 congeneric species of monogenean ectoparasites of fish on a molecular phylogeny of these species and found that the most highly host-specific species are not necessarily the more derived. This study is the only one to date performed within a robust phylogenetic context; because it is based on a single genus, however, the generality of its findings remains to be verified. It may not even be a common pattern among monogeneans in general. We need further tests carried out on a broader range of taxa, within a phylogenetic context.

Ideally, to test for evolutionary trends in host specificity among species of parasites, one would need to determine whether the host specificity of recent taxa is consistently different from that of ancestral taxa. Such a test is impossible because there is no information whatsoever on the host specificity of extinct parasite taxa; only extant taxa are available for analyses of evolutionary trends. Using phylogenetic information, however, it is possible to identify basal and derived taxa, i.e. taxa that have originated at different distances from the base of the tree (Pagel, 1997, Pagel, 1999, Pagel, 2002; Knouft and Page, 2003, Poulin, 2005a). Although this still does not provide information on the characteristics of extinct taxa, the host specificity of extant taxa gives an indication of how ancient and recent branches in the same phylogenetic tree have evolved since branching out.

Here, we examine evolutionary trends in host specificity of basal and derived species of fleas (Siphonaptera) parasitic on small mammals. Fleas usually alternate between periods when they occur on the body of their hosts and periods when they occur in their hosts' burrows or nests. The larvae are usually not parasitic and feed on organic debris in the burrow and/or nest of the host. The degree of association between a particular flea species and various host species varies, with flea species ranging from highly host-specific to host-opportunistic (Marshall, 1981). Our analyses allow both an assessment of general directional trends in the evolution of host specificity, as well as an evaluation of whether it is irreversible or not. We also test for consistent patterns among different genera and families of fleas, to assess the generality of any trend. The study makes use of a large data set on the host specificity of fleas, combined with phylogenetic information and robust analytical tools, to uncover phylogenetically correct statistical trends in the evolution of host specificity in parasitic organisms.