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Wolbachia in the Genus Bicyclus: a Forgotten Player

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Wolbachia in the Genus Bicyclus: a Forgotten Player Microb Ecol DOI 10.1007/s00248-017-1024-9 INVERTEBRATE MICROBIOLOGY Wolbachia in the Genus Bicyclus: a Forgotten Player Anne Duplouy1 & Oskar Brattström2 Received: 1 April 2017 /Accepted: 16 June 2017 # The Author(s) 2017. This article is an open access publication Abstract Bicyclus butterflies are key species for studies of Introduction wing pattern development, phenotypic plasticity, speciation and the genetics of Lepidoptera. One of the key endosymbi- Current estimates suggest that up to 70% of all insect species onts in butterflies, the alpha-Proteobacterium Wolbachia in the world may live in intimate relation with intracellular pipientis, is affecting many of these biological processes; micro-organisms [1, 2]. The outcome of such symbiotic asso- however, Bicyclus butterflies have not been investigated sys- ciations, or endosymbiosis, ranges from mutualistic and ben- tematically as hosts to Wolbachia.Inthisstudy,wescreenfor eficial to both the host and the microbe, to parasitic and detri- Wolbachia infection in several Bicyclus species from natural mental to the host [3]. The bacterial species Wolbachia populations across Africa as well as two laboratory popula- pipientis Hertig, 1936 [4], is one of the most common and tions. Out of the 24 species tested, 19 were found to be infect- best-studied endosymbionts found in insects. This maternally ed, and no double infection was found, but both A- and B- transmitted alpha-Proteobacterium selfishly promotes its own supergroup strains colonise this butterfly group. We also show fitness by manipulating several aspects of its host’s biology that many of the Wolbachia strains identified in Bicyclus but- [5]. The many potential distortions of the host’s fitness include terflies belong to the ST19 clonal complex. We discuss the the manipulation of its reproductive system [5] and of various importance of our results in regard to routinely screening for life-history traits, such as fecundity [6], dispersal [7] and re- Wolbachia when using Bicyclus butterflies as the study organ- sistance to stresses caused by pathogens or the environment ism of research in eco-evolutionary biology. [8]. In Drosophila simulans for example, the Wolbachia strain wRi causes karyogamy failure and the arrest of early embry- onic development of the offspring, when Wolbachia-free fe- Keywords Symbiosis . Butterfly . Bicyclus anynana . Model male flies are mated with Wolbachia-infected males [9]. organism However, at the same time, this bacterial strain protects the infected flies from viral infections [10]. By promoting its own Electronic supplementary material The online version of this article fitness, through increasing the fitness of the infected host lines (doi:10.1007/s00248-017-1024-9) contains supplementary material, compared to uninfected ones, Wolbachia has the potential to which is available to authorized users. act as a key player in the ecology and evolution of its hosts. Butterflies and moths have long fascinated and attracted the * Oskar Brattström [email protected] attention of entomologists, both professionals and amateurs. They are generally easily identified compared to many other Anne Duplouy insect groups, thus facilitating the documentation of their habits [email protected] and behaviors in natural environments. Furthermore, Lepidoptera often have relatively short life-cycles and high 1 Metapopulation Research Centre, Department of Biosciences, The University of Helsinki, PL65 Viikinkaari 1, fecundity, and many species can be reared continuously in lab- FI-00014 Helsinki, Finland oratory environments, thus making their use for large-scale 2 Department of Zoology, University of Cambridge, Downing Street, experiments feasible. Finally, with recent development of mo- Cambridge CB2 3EJ, UK lecular techniques, the study of insect genetics and genomics is Duplouy A., Brattström O. no longer restricted to the Drosophila scientific community. the standardised use of the five multilocus sequence typing The full genomes of 36 Lepidoptera are now publicly available markers (MLSTs [33]), and the genetic marker wsp [34]. For (see for example [11–15]), and more are in preparation or par- the first time, we show that Wolbachia infections are common tially sequenced (lepbase.org [16]). The availability of these in Bicyclus species, and that the strain diversity within this new tools combined with our extended knowledge of gene to host genus is relatively high. We discuss the potential impli- life-history traits, gained from both laboratory and field-based cations of these results for future studies using Bicyclus but- studies, makes many Lepidoptera species suitable model or- terflies as focal organisms. ganisms for ecology and evolutionary studies. There are over 100 species in the butterfly genus Bicyclus (Nymphalidae) [17]. Many species have distinct seasonal Material and Method morphs mediated through environmentally induced plasticity. These seasonal phenotypes are characterised by variations in Material wing patterns [18, 19], pheromone compounds [20]andvar- ious life-history traits [21, 22]. Oliver et al. [23] have, for The Bicyclus genus represents a highly diverse genus of over example, characterised different expression levels for several 100 African butterfly species [17]. The majority of the species genes involved in the regulation of the eyespot wing patterns inhabits the rainforest zone, while others are found in the between B. anynana specimens developing in different envi- savannah regions [35]. The many strikingly morphologically ronmental conditions, while Macias-Munoz et al. [24]have similar species in the genus are often only distinguishable shown that sexes and seasonal morphs differentially express through the comparison of highly divergent wing scales called several other genes involved in insect vision. Combined to- androconia, specialised structures at least partly linked to gether, these results suggest that the environment may play an pheromone production and release [36]. important role in both mate recognition and choice in In total, 200 specimens from 24 species across the genus Bicyclus. The imminent completion of the B. anynana full Bicyclus were used in this study [17] (Table 1). To avoid genome sequencing project (lepbase.org) will certainly lead phylogenetic bias, we included samples from all except one to an increased number of studies further investigating the (ena-group) of the 16 species groups currently recognised in consequences of seasonality in the evolutionary history of the genus [17]. Nineteen of the sampled species generally this and other Bicyclus species. inhabit forest environments, but some will also tolerate dry Despite the current wealth of eco-evolutionary studies on forest environments, while the remaining five are generally Bicyclus butterflies, and the fact that Wolbachia is a symbiont found in savannah habitats. Most species were collected from of many butterfly species worldwide [25], we are unaware of a wild populations between 2008 and 2012; however, study identifying the bacterium as an endosymbiont of B. anynana and B. safitza samples were collected in 2016 B. anynana, or of any other Bicyclus species. This knowledge from matrilines that had been maintained for several genera- gap currently clearly contrasts with our understanding of pecu- tions in the laboratory. The samples of B. anynana originated liar host-symbiont interactions in several related Nymphalidae from a stock of around 80 females collected in Malawi in 1988 butterflies. Wolbachia are for example present in various spe- and currently reared by many labs across the world. The sam- cies of Heteropsis [26], a genus closely related to Bicyclus [27], ples of B. safitza come from a more recent stock established andhavealsobeenassociatedwithCoenonympha tullia [28], from ten females collected in Uganda in 2013. The species Maniola jurtina [29], Caligo telamonius [30] and many other identities of our specimens were previously identified for the butterfly species [25 ]. Although further studies are needed to purpose of a phylogenetic study by Aduse-Poku et al. [17]. No fully characterise the effect of Wolbachia in their butterfly species of Bicyclus are currently classified as threatened spe- hosts, the currently available studies on symbiotic interaction cies, and all field-collected samples were collected with per- in a few butterfly species already suggest that the effects from mission from governmental organisations in their countries of such infections can have profound consequences for the eco- origin. For each species except one (see below), four to ten evolutionary biology of their butterfly hosts. The Wolbachia individuals were tested for infection by Wolbachia.Sincewe strains infecting the butterflies Hypolimnas bolina and Acraea focused on the screening of samples from a range of locations encedon, for example, kill the male progeny of infected female (up to five when possible) for each species, we potentially butterflies [31, 32], thus potentially limiting inbreeding and maximised the chance of detecting infections as well as strain sibling resource competition in these species. diversity per species, but not per population. Finally, since we In this paper, we report on the results from a screening for had no prior knowledge with regards to the induction of male presence of Wolbachia infections, and the diversity of the killing by endosymbionts in Bicyclus, we privileged female Wolbachia strains, in samples from natural populations of samples, but included males
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