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.2019 Jan 24;9(4):1736-1749.
doi: 10.1002/ece3.4846. eCollection 2019 Feb.

The Klingon batbugs: Morphological adaptations in the primitive bat bugs,Bucimex chilensis andPrimicimex cavernis, including updated phylogeny of Cimicidae

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The Klingon batbugs: Morphological adaptations in the primitive bat bugs,Bucimex chilensis andPrimicimex cavernis, including updated phylogeny of Cimicidae

Gonzalo Ossa et al. Ecol Evol..

Abstract

The Cimicidae is a family of blood-dependent ectoparasites in which dispersion capacity is greatly associated with host movements. Bats are the ancestral and most prevalent hosts for cimicids. Cimicids have a worldwide distribution matching that of their hosts, but the global classification is incomplete, especially for species outside the most common Cimicidae taxa. In this study, we place a little-studied cimicid species,Bucimex chilensis, within a comprehensive molecular phylogeny of Cimicidae by sequencing the genomic regions of this and other closely related species. For this study, we collectedB. chilensis females fromMyotis chiloensis in Tierra del Fuego, 1,300 km further south than previously known southernmost distribution boundary. We also sequenced COI regions fromPrimicimex cavernis, a species which together withB. chilensis comprise the entire subfamily Primiciminae. Using Bayesian posterior probability and maximum-likelihood approaches, we found thatB. chilensis andP. cavernis clustered close to each other in the molecular analyses, receiving support from similar morphological features, agreeing with the morphology-based taxonomic placement of the two species within the subfamily Primiciminae. We also describe a previously unrecognized morphological adaptation of the tarsal structure, which allows the austral bat ectoparasite,B. chilensis, to cling on to the pelage of its known host, the Chilean myotis (Myotis chiloensis). Through a morphological study and behavioral observation, we elucidate how this tarsal structure operates, and we hypothesize that by clinging in the host pelage,B. chilensis is able to disperse effectively to new areas despite low host density. This is a unique feature shared byP. cavernis, the only other species in Primiciminae.

Keywords: Chiroptera; Cimicinae; dispersal; ectoparasite; tarsal structure.

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Figures

Figure 1
Figure 1
Bucimex chilensis (white arrow) at the base of the tail, on the dorsal surface ofMyotis chiloensis
Figure 2
Figure 2
Map of austral South America. Previous collection sites ofBucimex chilensis are indicated with red dots. The present sample collection site is indicated with a red triangle
Figure 3
Figure 3
Dorsal and ventral views ofBucimex chilensis (left) andPrimicimex cavernis (right). Black arrow indicates spermalage onB. chilensis, which is missing fromP. cavernis
Figure 4
Figure 4
(a) Tarsal claws clinging on toMyotis chiloensis fur. (b) Tarsal claws and erect ctenidea (black arrow), which facilitate grasping host hair. (c) A similar tarsal structure onPrimicimex cavernis with ctenidea (black arrow). (d) The tibia and tarsi ofCimex lectulariarus with specialized setae on the joint (black arrow), which may be used to fasten the bug to the plagiopatagium of the bat
Figure 5
Figure 5
A multilocus DNA‐based phylogeny of Cimicidea using five genes with support values for all the main clades based on both Bayesian posterior probability (left number) and maximum‐likelihood analysis with 100 bootstrap replicates (right). Three Cimicomorpha families outside Cimicidae are used as an outgroup to root the tree. The higher taxa within Cimicoidea are marked in the clades. The morphological differences in the tarsi are illustrated for comparison:Orius niger (representing Anthocoridae and other outgroups),Bucimex chilensis(Primiciminae), andCimex lectularius (Cimicinae+Cacodminae)
Figure 6
Figure 6
A phylogeny of Cimicidea using COI gene with support values for all the main clades based on both Bayesian posterior probability (left number) and maximum‐likelihood analysis with 100 bootstrap replicates (right). Both Primiciminae species (B. chilensis andP. cavernis) cluster close to each other at the base of Cimicidae with high support. The subfamily Cacodminae is also strongly supported, but subfamily Cimicinae is poorly resolved, such as polyphyletic genusCimex
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