Competition promotes the evolution of host generalists in obligate parasites

Abstract

Ecological theory traditionally predicts that interspecific competition selects for an increase in ecological specialization. Specialization, in turn, is often thought to be an evolutionary 'dead end,' with specialist lineages unlikely to evolve into generalist lineages. In host-parasite systems, this specialization can take the form of host specificity, with more specialized parasites using fewer hosts. We tested the hypothesis that specialists are evolutionarily more derived, and whether competition favours specialization, using the ectoparasitic feather lice of doves. Phylogenetic analyses revealed that complete host specificity is actually the ancestral condition, with generalists repeatedly evolving from specialist ancestors. These multiple origins of generalists are correlated with the presence of potentially competing species of the same genus. A competition experiment with captive doves and lice confirmed that congeneric species of lice do, in fact, have the potential to compete in ecological time. Taken together, these results suggest that interspecific competition can favour the evolution of host generalists, not specialists, over macroevolutionary time.

The evolution of host specificity in dove body lice

“…1), we found that all gains of host generalists occurred in louse lineages found on doves that spend most of their time on the ground (concentrated changes test P = 0·037 over Bayesian tree, P = 0·022 over parsimony tree). There was no such correlation (P = 0·26) for wing lice when we repeated the analysis using data from Johnson et al (2009).…”

“…In contrast, host specialists do not disperse and/or establish on more than one host species. We coded the presence of a potentially competing species following Johnson et al (2009), using host association records from Price et al (2003) and additional associations represented in the published molecular data set (Johnson et al 2011).…”

“…Many species in each group parasitize only a single host species, although some species in each group parasitize more than one host species (Price et al 2003;Johnson et al 2009). These differences in host specificity may, in part, be determined by differences in dispersal ability.…”

Synthesizing Parasitology with Archaeology in Paleopathology

“…The other hundreds of helminth species that infect humans also infect other host species. Most recently, Johnson et al (2009) presented phylogenetic and experimental support of the hypothesis that host specificity is an ancestral condition. Generalists evolved from specialist ancestors.…”

Specific and Nonspecific Host Adaptation during Arboviral Experimental Evolution

“…For example, host specificity of phage ⌽ -6 depends largely on receptor recognition, and the virus seems unable to produce a protein that can recognize multiple bacterial receptors simultaneously, so adaptation to new hosts usually results in loss of recognition of the old host receptor [Ferris et al, 2007]. Some environmental conditions may have an effect on the selection of specialists or generalists, such as interspecies competition [Johnson et al, 2009], coevolution with the host [Hall et al, 2011], or the supply of beneficial variation [Jasmin and Kassen, 2007], which does not seem to be limiting in RNA viruses [Betancourt, 2009;Bollback and Huelsenbeck, 2007;Dutta et al, 2008]. While there are some arguments as to whether true generalists exist in nature [Loxdale et al, 2011], arboviruses are usually considered the ultimate generalists due to their potential to replicate and perform well in a wide variety of hosts [Weaver, 2006].…”