On the diversification of highly host-specific symbiontsThe case of feather mites

Resumen

One of the most relevant and poorly understood topics in Evolutionary Ecology is symbiont evolutionary diversification. Since Fahrenholz's rule (1913), the idea of symbionts speciating following hosts speciation (i.e., cospeciating) has been pervasive. Recent studies, however, have shown that host-shift speciation (speciation after switching to a new host) is almost as relevant as cospeciation in explaining symbiont diversification. Also, these studies have revealed that methodological biases have favored cospeciation. Nonetheless, most symbiont groups, especially those highly host-specific and specialized in which cospeciation is expected to be the rule, such as the feather mites of birds, were yet to be studied. Symbionts are the most abundant and diverse organisms on Earth, and thus essential components of ecosystems. However, symbionts have attracted historically less attention than other organisms and their study entails numerous methodological challenges, so surprisingly little is understood about the basic biology and ecology of many symbiont groups, especially the non-parasitic. By studying vane-dwelling feather mites living permanently on the surface of flight feathers of birds (Acariformes: Astigmata: Analgoidea and Pterolichoidea), this thesis is a contribution to fill this gap. This thesis is divided into three parts: 1) First, resources and molecular tools enabling large-scale studies of feather mites are developed. 2) Then, these and other tools are used to investigate eco-evolutionary aspects relevant to understand feather mite diversification, such as their mode of transmission and the type of interaction they have with their hosts. 3) Finally, feather mites diversification at a macro- and microevolutionary scale is investigated. The first part compiles a global database of bird-feather mites associations. Also, it evaluates and adjusts DNA barcoding and metabarcoding to be suitable methodologies for studying feather mites. The second part reveals feather mites as highly specialist and hostspecific symbionts whose main mode of transmission is vertical. Analyses of feather mites diet reveal them as trophic generalists which maintain a commensalistic-mutualistic relationship with birds. Finally, the last part of the thesis shows host-shift speciation as the primary process driving the diversification of feather mites. Also, it highlights that majorhost switching, despite being an infrequent process, is highly relevant for the diversification of this group. Lastly, analyses of straggling reveal a high rate of preferential straggling governed by ecological filters. Overall, despite feather mites are revealed as highly specialized and host-specific symbionts, the coevolutionary scenario is highly dynamic. Straggling and host-switching are prevalent processes which allow colonizing new hosts in highly specialized and hostspecific symbionts. Accordingly, coevolution and codiversification do not operate in isolated host-symbiont interactions but more likely in a manner compatible with the geographic mosaic of coevolution. Finally, ecological fitting and interspecific competition are most likely the main factors governing the (co)eco-evolutionary dynamics.