Cophylogenetic analyses reveal extensive host-shift speciation in a highly specialized and host-specific symbiont system

Doña, Jorge; Sweet, Andrew D.; Johnson, Kevin P.; Serrano, David; Mironov, Sergey V.; Jovani, Roger

doi:10.1016/j.ympev.2017.08.005

Cited by 46 publications

(44 citation statements)

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“…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.…”

Section: Discussionsupporting

confidence: 81%

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

et al. 2019

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The high relevance of host‐switching for the diversification of highly host‐specific symbionts (i.e., those commonly inhabiting a single host species) demands a better understanding of host‐switching dynamics at an ecological scale. Here, we used DNA metabarcoding to study feather mites on passerine birds in Spain, sequencing mtDNA (COI) for 25,540 individual mites (representing 64 species) from 1,130 birds (representing 71 species). Surprisingly, 1,228 (4.8%) mites from 84 (7.4%) birds were found on host species that were not the expected to be a host according to a recent bird–feather mite associations catalog. Unexpected associations were widespread across studied mite (40.6%) and bird (43.7%) species and showed smaller average infrapopulation sizes than typical associations. Unexpected mite species colonized hosts being distantly related to the set of their usual hosts, but with similar body size. The network of bird–mite associations was modular (i.e., some groups of bird and mite species tended to be more associated with each other than with the others), with 75.9% of the unexpected associations appearing within the module of the typical hosts of the mite species. Lastly, 68.4% of mite species found on unexpected hosts showed signatures of genetic differentiation, and we found evidence for reproduction or the potential for it in many of the unexpected associations. Results show host colonization as a common phenomenon even for these putatively highly host‐specific symbionts. Thus, host‐switching by feather mites, rather than a rare phenomenon, appears as a relatively frequent phenomenon shaped by ecological filters such as host morphology and is revealed as a fundamental component for a dynamic coevolutionary and codiversification scenario.

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Section: Discussionsupporting

confidence: 81%

“…We found phylogenetic information for all the bird species we studied. Following Doña, Sweet, et al (), Avibase information (accessed on March 2016; Lepage et al, ) was used to match avian taxonomy in Doña et al () with that of Jetz et al ().…”

Section: Methodsmentioning

confidence: 99%

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

et al. 2019

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“…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., ).…”

Section: Discussionmentioning

confidence: 99%

“…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, ).…”

Section: Introductionmentioning

confidence: 99%

Feather mites play a role in cleaning host feathers: New insights from DNA metabarcoding and microscopy

et al. 2018

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Parasites and other symbionts are crucial components of ecosystems, regulating host populations and supporting food webs. However, most symbiont systems, especially those involving commensals and mutualists, are relatively poorly understood. In this study, we have investigated the nature of the symbiotic relationship between birds and their most abundant and diverse ectosymbionts: the vane-dwelling feather mites. For this purpose, we studied the diet of feather mites using two complementary methods. First, we used light microscopy to examine the gut contents of 1,300 individual feather mites representing 100 mite genera (18 families) from 190 bird species belonging to 72 families and 19 orders. Second, we used high-throughput sequencing (HTS) and DNA metabarcoding to determine gut contents from 1,833 individual mites of 18 species inhabiting 18 bird species. Results showed fungi and potentially bacteria as the main food resources for feather mites (apart from potential bird uropygial gland oil). Diatoms and plant matter appeared as rare food resources for feather mites. Importantly, we did not find any evidence of feather mites feeding upon bird resources (e.g., blood, skin) other than potentially uropygial gland oil. In addition, we found a high prevalence of both keratinophilic and pathogenic fungal taxa in the feather mite species examined. Altogether, our results shed light on the long-standing question of the nature of the relationship between birds and their vane-dwelling feather mites, supporting previous evidence for a commensalistic-mutualistic role of feather mites, which are revealed as likely fungivore-microbivore-detritivore symbionts of bird feathers.

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“…Given this biology, it is surprising that a recent cophylogenetic study between two genera of feather mites and European passerine birds (Doña, Sweet, Johnson, Serrano, & Jovani, ) showed that host switching, rather than host–parasite cospeciation (i.e., symbiont speciation after host speciation), may be the main driver of diversification. In fact, cophylogenetic reconstructions showed that speciation after host switching was more prevalent by far than cospeciation in the passerine feather mites studied.…”

Section: Introductionmentioning

confidence: 99%

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

Doña

Proctor

Mironov

et al. 2017

Global Ecol Biogeogr

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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.

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Cophylogenetic analyses reveal extensive host-shift speciation in a highly specialized and host-specific symbiont system

Cited by 46 publications

References 80 publications

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

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

Feather mites play a role in cleaning host feathers: New insights from DNA metabarcoding and microscopy

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

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