Persistence of single species of symbionts across multiple closely-related host species

Abstract

Some symbiont species are highly host-specific, inhabiting only one or a very few host species, and typically have limited dispersal abilities. When they do occur on multiple host species, populations of such symbionts are expected to become genetically structured across these different host species, and this may eventually lead to new symbiont species over evolutionary timescales. However, a low number of dispersal events of symbionts between host species across time might be enough to prevent population structure and species divergence. Overall, processes of evolutionary divergence and the species status of most putative multi-host symbiont systems are yet to be investigated. Here, we used DNA metabarcoding data of 6,023 feather mites (a total of 2,225 OTU representative sequences) from 147 infracommunities (i.e., the assemblage consisting of all mites of different species collected from the same bird host individual) to investigate patterns of population genetic structure and species status of three different putative multi-host feather mite species Proctophyllodes macedo Vitzthum, 1922, Proctophyllodes motacillae Gaud, 1953, and Trouessartia jedliczkai (Zimmerman, 1894), each of which inhabits a variable number of different closely related wagtail host species (genus Motacilla). We show that mite populations from different host species represent a single species. This pattern was found in all the mite species, suggesting that each of these species is a multi-host species in which dispersal of mites among host species prevents species divergence. Also, we found evidence of limited evolutionary divergence manifested by a low but significant level of population genetic structure among symbiont populations inhabiting different host species. Our study agrees with previous studies showing a higher than expected colonization opportunities in host-specific symbionts. Indeed, our results support that these dispersal events would allow the persistence of multi-host species even in symbionts with limited dispersal capabilities, though additional factors such as the geographical structure of some bird populations may also play a role.

Sex and age‐class differences in feather mite loads in white wagtailsMotacilla alba lugenssuggest self‐regulation of feather mites by birds

“…Recent information about the behaviour of feather mites has shown that feather mites are most active at night (Labrador et al 2021b). Although most feather mite species show a high degree of host specificity (Proctor 2003, Doña et al 2017), three different species of wagtails have been found hosting the same mite species (Doña et al 2019), which is indicative of horizontal transmission. If horizontal transmission of mites between wagtails sharing roosting sites is occurring (i.e.…”

Assessing symbiont extinction risk using cophylogenetic data

“…generally yield the highest adaptive potential (Allendorf et al, 2007;Futuyma, 2013). Most symbiont species have levels of gene flow between populations that are often higher than between host populations, and therefore extreme levels of population subdivision are not expected to be the norm (Clayton et al, 2015;Doña et al, 2019a;Huyse et al, 2005;Mazé-Guilmo et al, 2016;McCoy et al, 2003;. However, symbiont populations are theoretically expected to become more fragmented due to anthropogenic causes (Pickles et al, 2013;Carlson et al, 2017a), leading to situations in which worrisome levels of subdivision can become more frequent.…”

“…This result agrees with existing comparative knowledge from the ecology and evolution of these mites. Specifically, Trouessartia mites are known to have: 1) a lower species diversity on Passeriformes (Doña et al, 2016(Doña et al, , 2018, 2) lower prevalence (i.e., the proportion of individuals inhabited by a symbiont species within a host sample; Reiczigel et al, 2019) and intensity (i.e., the number of individual symbionts inhabiting a particular host; Reiczigel et al, 2019) (Fernández-González et al, 2018Doña et al, 2019b), 3) lower genetic diversity (Fernández-González et al, 2018;Doña et al, 2019b), and 4) infrapopulations genetically more structured (i.e., with lower gene flow among infrapopulations -all the individual symbionts inhabiting an individual host-, than Proctophyllodes species (Doña et al, 2019a).…”

Male‐biased dispersal in a fungus‐gardening ant symbiosis

“…Dispersal can shape population genetic differentiation, overall species distributions, and how species may respond or adapt to environmental change (Clobert et al., 2012; Ellis et al., 2015). For species with low dispersal capabilities, historical, ecological, or anthropogenic barriers to movement can influence their population genetic structure over certain scales (Doña et al., 2019; Haye et al., 2014; Manel et al., 2003; Storfer et al., 2010). For example, barriers may slow gene flow between some populations, increase reproductive and genetic isolation and ultimately result in genetically divergent populations (Clark et al., 2010; DiBlasi et al., 2018; Slatkin, 1987).…”