Geography and major host evolutionary transitions shape the resource use of plant parasites

Abstract

The evolution of resource use in herbivores has been conceptualized as an analog of the theory of island biogeography, assuming that plant species are islands separated by phylogenetic distances. Despite its usefulness, this analogy has paradoxically led to neglecting real biogeographical processes in the study of macroevolutionary patterns of herbivore-plant interactions. Here we show that host use is mostly determined by the geographical cooccurrence of hosts and parasites in spider mites (Tetranychidae), a globally distributed group of plant parasites. Strikingly, geography accounts for most of the phylogenetic signal in host use by these parasites. Beyond geography, only evolutionary transitions among major plant lineages (i.e., gymnosperms, commelinids, and eudicots) shape resource use patterns in these herbivores. Still, even these barriers have been repeatedly overcome in evolutionary time, resulting in phylogenetically diverse parasite communities feeding on similar hosts. Therefore, our results imply that patterns of apparent evolutionary conservatism may largely be a byproduct of the geographic cooccurrence of hosts and parasites.evolutionary conservatism | geographic signal | host use evolution | parasite-host interactions | spider mites E cological interactions are commonly thought to be evolutionarily conserved (1). This idea roots back to Darwin and is based on the assumption that traits regulating interactions are mainly an ancestor's legacy. Following this rationale, it is expected that phylogenetically related species will also interact with partners that are phylogenetically clustered. Plants and the herbivores that feed on them constitute a large amount of the Earth's terrestrial biodiversity. However, the processes behind the origin of such diversity remain controversial (2). Related plant hosts tend to harbor similar communities of both herbivores (3-5) and pathogens (6, 7). Still, host shifts may be favored when they involve distantly related plants producing similar chemical compounds as defense against parasites (8). In fact, macroevolutionary evidence shows that host shifts of parasites to unrelated plants are common (9-13), questioning the ubiquity of evolutionary conservatism.These patterns of host use in parasites have led to the formulation of the "parasite paradox," which states that although parasites are generally specialized on a given (set of) host plant(s), host shifts to distantly related hosts occur frequently (14, 15). Further, the frequent shifts between evolutionarily distinct hosts observed in parasites have led to the analogy of considering plant species as resource islands separated by evolutionary distances (16)(17)(18). In this metaphor, related plants constitute resource archipelagos within which colonization of new resource islands entails few costs. Among such archipelagos, however, colonization processes may be costly, potentially leading to disruptive selection and hence to speciation via host shift (19,20). Paradoxically, framing the evolution of plant host use ...

Host specificity, infrequent major host switching and the diversification of highly host‐specific symbionts: The case of vane‐dwelling feather mites

“…Altogether, our results depict feather mites as strongly limited by transmission opportunities or highly constrained by finding similar ecological conditions on the new host, as suggested by mite species inhabiting hosts with a close phylogenetic relationship (see also Agosta & Klemens, ; Agosta, Janz, & Brooks, ; Araujo et al, ; Combes, ; Khokhlova, Fielden, Degen, & Krasnov, ; Poulin, ). Interestingly, the opposite pattern has been reported for other symbionts with much higher dispersal capabilities than feather mites, such as rodent fleas (Krasnov et al, ), tapeworm fish parasites (Bouzid et al, ) and, recently, for spider mite symbionts of plants (Calatayud et al, ). Indeed, these contrasting results within mites support that major host switches are particularly unexpected in highly specialized symbionts.…”

“…For example, the arrival of new insect species on oceanic islands, or the long‐distance dispersal of plant seeds, can result in major consequences for evolutionary radiations and global biogeography (Darwin, ; Nathan, ). Host switching (the successful colonization of a new host species by a symbiont species) falls into this category; switches are rare and difficult to detect, but because successful switches can isolate symbiont populations in new ecological contexts, they have a high potential to drive diversification of symbionts (Calatayud et al, ; Clayton, Bush, & Johnson, ; de Vienne et al, ; Hoberg & Brooks, ; Johnson, Weckstein, Meyer, & Clayton, ; Martinů et al, ; Nyman, ; Poulin, ; Ricklefs et al, ). Although symbionts constitute much of Earth's biodiversity (Dobson, Lafferty, Kuris, Hechinger, & Jetz, ; Larsen, Miller, Rhodes, & Wiens, ; Morand, ), we still lack a solid understanding of host‐switching dynamics and how it shapes symbiont evolution.…”

“…Nevertheless, one general pattern shared among symbionts is that successful switches occur mainly between phylogenetically closely related hosts (‘clade‐limited switches’; Braga, Razzolin, & Boeger, ; Krasnov, Poulin, Shenbrot, Mouillot, & Khokhlova, ; Krasnov et al, ; Poulin, ; Poulin, Krasnov, & Mouillot, ). However, on rare occasions, symbionts may establish on phylogenetically distant hosts (‘major host switches’; Calatayud et al, ; Johnson, Weckstein, Meyer et al, ; Martinů et al, ; Nyman, ; Poulin, ; Torchin, Lafferty, Dobson, McKenzie, & Kuris, ). Subsequent speciation on the new host can initiate a co‐evolutionary radiation (Clayton et al, ).…”

Unifying macroecology and macroevolution to answer fundamental questions about biodiversity

“…This finding has been interpreted as evidence of environmental filtering acting on the community of parasites at the “macro” scale (Krasnov et al, ). On the other hand, there is evidence that differences in parasite communities across hosts are driven by parasite geographical ranges and not phylogenetic distance, despite a strong apparent signal of phylogenetic conservatism [Calatayud et al, ; also see similar results in insect–host associations (Nylin et al, )]. The field of community phylogenetics also touches on interactions between species based on the amount of their shared evolutionary history (Cavender‐Bares, Ackerly, Baum, & Bazzaz, ; Webb et al, 2002; but see cautions in Mayfield & Levine, ).…”

A phylogenetic comparative method for evaluating trait coevolution across two phylogenies for sets of interacting species

“…; Calatayud et al. ). Likewise, some methods model phenotypic evolution of continuous characters in one lineage while taking into consideration changes in trait values in a second set of coevolving taxa that interact with the focal clade (Manceau et al.…”