Cophylogenetic assessment of New World warblers (Parulidae) and their symbiotic feather mites (Proctophyllodidae)

Abstract

Host–symbiont relationships are ubiquitous in nature, yet evolutionary and ecological processes that shape these intricate associations are often poorly understood. All orders of birds engage in symbioses with feather mites, which are ectosymbiotic arthropods that spend their entire life on hosts. Due to their permanent obligatory association with hosts, limited dispersal and primarily vertical transmission, we hypothesized that the cospeciation between feather mites and hosts within one avian family (Parulidae) would be perfect (strict cospeciation). We assessed cophylogenetic patterns and tested for congruence between species in two confamiliar feather mite genera (Proctophyllodidae: Proctophyllodes, Amerodectes) found on 13 species of migratory warblers (and one other closely related migratory species) in the eastern United States. Based on COI sequence data, we found three Proctophyllodes lineages and six Amerodectes lineages. Distance‐ and event‐based cophylogenetic analyses suggested different cophylogenetic trajectories of the two mite genera, and although some associations were significant, there was little overall evidence supporting strict cospeciation. Host switching is likely responsible for incongruent phylogenies. In one case, we documented prairie warblers Setophaga discolor harboring two mite species of the same genus. Most interestingly, we found strong evidence that host ecology may influence the likelihood of host switching occurring. For example, we documented relatively distantly related ground‐nesting hosts (ovenbird Seiurus aurocapilla and Kentucky warbler Geothlypis formosa) sharing a single mite species, while other birds are shrub/canopy or cavity nesters. Overall, our results suggest that cospeciation is not the case for feather mites and parulid hosts at this fine phylogenetic scale, and raise the question if cospeciation applies for other symbiotic systems involving hosts that have complex life histories. We also provide preliminary evidence that incorporating host ecological traits into cophylogenetic analyses may be useful for understanding how symbiotic systems have evolved.

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.…”

“…Thus, such host‐specific symbionts have all the ingredients to be diversifying mainly by cospeciation. Interestingly, and contrary to this expectation, there is also evidence of horizontal transfer within and between bird species (Dubinin, ; Gaud, ; Jovani & Blanco, ), and recent studies have inferred that host‐switching with subsequent speciation is the primary process driving their evolutionary diversification (Doña, Sweet, et al, ; Doña, Proctor, Mironov, et al, ; Klimov et al, ; Matthews et al, ). These results suggest that host‐switching, despite its apparent difficulty for feather mites, has left macroevolutionary fingerprints along millions of years (Doña, Proctor, Mironov, et al, ; Doña, Sweet, et al, ).…”

“…Moreover, even for putatively highly host-specific symbionts such as feather mites on birds, they have been often described as multihost (or oligoxenous) symbionts (Dabert, Solarczyk, Badek, & Dabert, 2005;Doña, Proctor, Mironov, Serrano, & Jovani, 2018), and there are some evidence supporting that straggling and eventual host-switching to a new host may be a common phenomenon (Doña, Sweet, et al, 2017;Doña, Proctor, Mironov, et al, 2018;Gaud, 1992;Klimov, Mironov, & OConnor BM, 2017;Matthews et al, 2018). However, we are still far from quantifying the relevance of these processes and understanding the mechanisms governing them.…”

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., ).…”

“…Lastly, a hypothesis of an "external-rumen" mode of feeding, in which mites ingest predigested food (by bacteria), has been also supported in free-living astigmatan mites (Hubert et al, 2014(Hubert et al, , 2016 and would be also compatible with our results. of switching to new host species (Doña, Proctor, et al, 2017;Doña, Sweet, et al, 2017;Gaud 1992;Klimov, Mironov, & O'Connor, 2017;Matthews et al, 2018). 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, 2017).…”