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

Abstract

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.

Comparing rates of introgression in parasitic feather lice with differing dispersal capabilities

“…This work is among the first studies of introgression in a host-symbiont system (Detwiler and Criscione 2010). Notably, recent studies have found that straggling and host-switching are relatively common processes in host-symbiont systems (De Vienne et al 2013;Bourguignon et al 2018;Nylin et al 2018;Doña et al 2019). Our study suggests that in a straggling/host-switching scenario, hybridization can provide further genetic variation with important ecological and evolutionary consequences (e.g., facilitating adaptation to current hosts or facilitating the colonization of new ones) (Barton 2018).…”

Introduction: Special issue on species interactions, ecological networks and community dynamics – Untangling the entangled bank using molecular techniques

“…The findings regarding particular interactions range from insight into emergent features such as levels of specialization in ecological interaction networks (Clare et al, ; Doña, Proctor, et al, ; Doña, Serrano, et al, ; Koskinen et al, ; Sepp et al, ) to the role of individual seed dispersers in seed dispersal networks. As a case in point, González‐Varo, Arroyo, and Jordano () are able to show how much of an ecological function (seed dispersal) is concentrated to particular species at particular points in time.…”

“…Doña, Serrano, et al () take an evolutionary perspective by examining the evidence for host shifts among symbionts presumed to be highly host‐specific. Building on extensive DNA metabarcoding, these authors study associations between nodes consisting of feather mite species and host bird species, finding much more variation in link structure than previously assumed.…”

“…In evidence of these claims, Doña, Proctor, et al () use high‐throughput sequencing (HTS) and DNA metabarcoding to determine gut contents from 1,833 individual mites of 18 species inhabiting 18 bird species, whereas Doña, Serrano, et al () report findings from 25,540 individual mites (representing 64 species) from 1,130 birds (representing 71 species). Tiusanen et al () sampled 31,345 arthropods, of which they individually sequenced 13,681 individuals, detecting 1,360 barcoding BINs in the process.…”

Assessing symbiont extinction risk using cophylogenetic data

“…Symbionts, defined as parasites, mutualists, and commensals that interact intimately with their 35 hosts (Leung and Poulin, 2008), are highly relevant components of ecosystems, comprising up to 36 75% of all ecological interactions (Lafferty et al, 2006;Dobson et al, 2008). A major concern is 37 that conservative estimates predict that a high percentage of symbiont species are expected to go 38 extinct due to climate change (e.g., 10 % of parasite species by 2070, Carlson et al, 2017a; Dunn frequent at an ecological scale, whereas successful host-switches (i.e., not only reaching a new 152 host but also reproducing on the new host) are comparatively rare (Whiteman et al, 2004;Rivera-153 Parra et al, 2017; Doña et al, 2019bDoña et al, , 2018. Higher straggling and host-switching capabilities 154 might be associated with a higher likelihood of escaping from host extinctions (Agosta et al, 2010; 155 Agosta and Klemens, 2008; Clayton et al, 2015;Engelstädter and Fortuna, 2019).…”