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

Abstract

Aim Highly host‐specific symbionts are very rarely found except with their typical host species. Although switches to new hosts are rare and difficult to detect, a switch to a host phylogenetically distant from the original one (a ‘major host switch’) could allow diversification of the symbionts onto the new host lineage. The consequences of such major host switches on the diversification of highly host‐specific symbionts of animals have rarely been explored. Here, we examine the host specificity of vane‐dwelling feather mites, a group that shows strong specificity, together with their host‐switching dynamics and the consequences of major host switches for their diversification. Location Global. Time period From 1882 to 2015. Major taxa studied Feather mites and birds. Methods Using the largest published dataset of feather mite–bird associations, we analysed raw, phylogenetic and geographical host specificity of feather mites. We studied host‐switching dynamics by describing the sharing by feather mites of bird species with different phylogenetic distances. For three of the most species‐rich feather mite families, we quantified the consequences of major host switches for feather mite diversification. Results Most feather mite species (84%) inhabit one to three very closely related host species. Assemblages of feather mites on birds do not show a geographical signature, but rather show strong host‐driven structuring. The probability that a mite species occurs on two host species decays sharply with host phylogenetic distance, with only one instance of a feather mite species occupying distantly related hosts from different orders. However, results suggest that despite the strong host specificity, a few major host switches triggered the origin of 21% of the species and 38% of the genera of the mite families studied. Main conclusions We show that feather mites are highly host‐specific symbionts, whose assemblages do not show geographical structure, even at a continental scale. We conclude that major host switches are very rare events with strong macroevolutionary consequences for feather mite diversity.

Unexpected bird–feather mite associations revealed by DNA metabarcoding uncovers a dynamic ecoevolutionary scenario

“…Lack of bird–feather mites phylogenetic congruence (at low taxonomic ranks) and the power of host‐switching to trigger further diversification have been shown elsewhere (Doña, Sweet, et al, ; Doña, Proctor, Mironov, et al, ; Matthews et al, ), and here, we provide evidence on how these patterns emerge from processes occurring at ecological and microevolutionary scales. Perhaps more importantly, a highly dynamic ecoevolutionary scenario where macroevolutionary patterns are only one of its outcomes is depicted, demanding to focus on the dynamics of these unexpected associations.…”

“…However, specifically, these hosts were more distantly related to the typical hosts than expected according to the phylogenetic host specificity of typical bird–feather mite associations (Figure ). And this degree of relatedness was partially overlapping with the longest phylogenetic distances reported for typical associations in Doña, Proctor, Mironov, et al () (Figure ). Finally, these unexpected associations were found in hosts with phylogenetic distances much shorter than potential associations with other bird species found in the same localities (e.g., mite species coming from non‐passerine birds of the study localities would have introduced hosts in the analysis which would have shown phylogenetic distances above 100 in Figure ).…”

Feather mites play a role in cleaning host feathers: New insights fromDNAmetabarcoding and microscopy

“…Feather mite species are relatively host‐specific and (presumably) host‐specialized symbionts that appear to have relatively low levels of switching to new host species (Doña, Proctor, et al., ; Doña, Sweet, et al., ; Gaud ; Klimov, Mironov, & O'Connor, ; Matthews et al., ). These switches mostly involve closely related hosts, but major‐host switches (e.g., between bird orders) have been revealed as a major driver of their diversification (Doña, Proctor, et al., ). As for many other host–symbiont systems (Clayton, Bush, & Johnson, ; Nylin et al., ), understanding the (co)eco‐evolutionary scenario of host‐switching in this host–symbiont system is still in its infancy.…”

“…Almost all bird species harbour species‐ or genus‐specific feather mites (Doña, Proctor, Mironov, Serrano, & Jovani, ; Gaud & Atyeo, ; Proctor, ). Feather mites are highly specialized symbionts due to their (i) life cycle (i.e., they are permanent ectosymbionts, Dabert & Mironov, ; Proctor, ); (ii) high host specificity (Doña, Proctor, Mironov, Serrano, & Jovani, ); (iii) specific distribution on particular feathers and microsites on feathers (Fernández‐González, Pérez‐Rodríguez, de la Hera, Proctor, & Pérez‐Tris, ; Jovani & Serrano, , ; Stefan et al., ); and (iv) mainly vertical mode of transmission (Doña, Potti, et al., ; Jovani, Tella, Sol, & Ventura, ; Mironov & Malyshev, ). However, as with many other symbionts, they are challenging to study, and this has strongly hampered our comprehension of this system (Doña, Diaz‐Real, et al., ; Proctor, ; Proctor & Owens, ).…”

Global patterns in helminth host specificity: phylogenetic and functional diversity of regional host species pools matter

“…Yet, to our knowledge, few studies of parasite host specificity across biogeographical scales account for variation in available hosts (Krasnov et al 2004, Cooper et al 2012, Lootvoet et al 2013, Doña et al 2017, Poisot et al 2017. Yet, to our knowledge, few studies of parasite host specificity across biogeographical scales account for variation in available hosts (Krasnov et al 2004, Cooper et al 2012, Lootvoet et al 2013, Doña et al 2017, Poisot et al 2017.…”