Redundant species, cryptic host-associated divergence, and secondary shift in Sennertia mites (Acari: Chaetodactylidae) associated with four large carpenter bees (Hymenoptera: Apidae: Xylocopa) in the Japanese island arc.

Sennertia mites live as inquilines in the nests of carpenter bees and disperse as deutonymphs on newly emerged adult bees. Because their life cycle is tightly linked to that of the host bees, Sennertia may diverge in response to speciation in the hosts. However, the majority of Sennertia species are associated with several closely related carpenter bees, suggesting that host speciation may not be reflected in mite genetic structure. Here we investigate the extent of host-associated genetic differentiation in two Sennertia mites (S. alfkeni and S. japonica) that share four closely related, strictly allopatric large carpenter bees (Xylocopa). Analysis of the mitochondrial cytochrome oxidase subunit I (COI) gene in Sennertia unexpectedly indicates that the two species represent morphological variants of a single species, and they collectively group into four distinct, allopatric clades that are uniquely associated with a single Xylocopa host. An exception is the mites associated with X. amamensis of the northernmost populations, which have genotypes typical of those associated with neighboring X. appendiculatacircumvolans. Additional analysis using amplified fragment length polymorphism (AFLP) further corroborates the presence of four mite clades but contrary to the COI data, suggests that the mites of the southernmost population of X. appendiculatacircumvolans have genetic profiles typical of those associated with X. amamensis. These results indicate that some mites have undergone secondary host switch after the formation of the four mite lineages and further experienced mitochondrial introgression during period of lineage coexistence. Overall, our results strongly urge reappraisal of deutonymph-based mite taxonomy and illuminate the importance of host-associated divergence during incipient stage of speciation in chaetodactylid mites. Furthermore, the occurrence of host switch and introgression between genetically differentiated mites entails that two host species have co-occurred in the past, thus providing a unique source of evidence for migration and competitive exclusion between the presently allopatric Xylocopa hosts.