Abstract

Host–parasite coevolution stems from reciprocal selection on host resistance and parasite infectivity, and can generate some of the strongest selective pressures known in nature. It is widely seen as a major driver of diversification, the most extreme case being parallel speciation in hosts and their associated parasites. Here, we report on endoparasitic nematodes, most likely members of the mermithid family, infecting different Timema stick insect species throughout California. The nematodes develop in the hemolymph of their insect host and kill it upon emergence, completely impeding host reproduction. Given the direct exposure of the endoparasites to the host's immune system in the hemolymph, and the consequences of infection on host fitness, we predicted that divergence among hosts may drive parallel divergence in the endoparasites. Our phylogenetic analyses suggested the presence of two differentiated endoparasite lineages. However, independently of whether the two lineages were considered separately or jointly, we found a complete lack of codivergence between the endoparasitic nematodes and their hosts in spite of extensive genetic variation among hosts and among parasites. Instead, there was strong isolation by distance among the endoparasitic nematodes, indicating that geography plays a more important role than host‐related adaptations in driving parasite diversification in this system. The accumulating evidence for lack of codiversification between parasites and their hosts at macroevolutionary scales contrasts with the overwhelming evidence for coevolution within populations, and calls for studies linking micro‐ versus macroevolutionary dynamics in host–parasite interactions.

Highlights

  • Parasites are ubiquitous in nature and are known to play a fundamental role in community ecology and the evolution of the hosts they infect (e.g., Thompson 1994; Bohannan and Lenski 2000; Woolhouse et al 2002; Decaestecker et al 2005; Schmid-Hempel 2011)

  • Ecology and Evolution published by John Wiley & Sons Ltd

  • We found mermithid-like endoparasitic nematodes in nine different Timema stick insect species, which prompted us to test for codiversification of these nematodes and their hosts

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Summary

Introduction

Parasites are ubiquitous in nature and are known to play a fundamental role in community ecology and the evolution of the hosts they infect (e.g., Thompson 1994; Bohannan and Lenski 2000; Woolhouse et al 2002; Decaestecker et al 2005; Schmid-Hempel 2011). Host defense mechanisms are generally detrimental for parasites, leading to selection for counteradaptations in the parasites. Host– parasite coevolution stems from reciprocal selection on host resistance and parasite infectivity (e.g., Thompson 1994; Ebert 1998; Clayton et al 1999; Carius et al 2001; Dybdahl et al 2014). Evidence that coevolutionary interactions drive evolutionary changes stems from taxonomically diverse host systems, including bacteria (e.g., Weitz et al 2005), plants (e.g., Dodds and Rathjen 2010; Karasov et al 2014), invertebrates (e.g., Decaestecker et al 2007; Ebert 2008), and vertebrates (Kerr 2012). Host–parasite coevolution is widely seen as a major driver of diversification, the most extreme case being codiversification or parallel speciation in hosts and their associated parasites (e.g., Clarke 1976; Price 1980; Kiester et al 1984; Buckling and Rainey 2002; Thompson et al 2005; Nieberding and Morand 2006; Ricklefs 2010; Yoder and Nuismer 2010; Weber and Agrawal 2012; Masri et al 2015)

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