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Wolbachia host shifts: routes, mechanisms, constraints and evolutionary consequences Ehsan Sanaei, Sylvain Charlat, Jan Engelstädter To cite this version: Ehsan Sanaei, Sylvain Charlat, Jan Engelstädter. Wolbachia host shifts: routes, mechanisms, con- straints and evolutionary consequences. Biological Reviews, Wiley, 2020, 10.1111/brv.12663. hal- 03076872 HAL Id: hal-03076872 https://hal-cnrs.archives-ouvertes.fr/hal-03076872 Submitted on 5 Jan 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Wolbachia host shifts: routes, mechanisms, constraints and evolutionary consequences Ehsan Sanaei1, Sylvain Charlat2 & Jan Engelstädter1 1 School of Biological Sciences, The University of Queensland, Brisbane, Australia 2 Université de Lyon, Université Lyon 1, CNRS, UMR 5558, Laboratoire de Biométrie et Biologie Evolutive, 43 boulevard du 11 novembre 1918, Villeurbanne F- 69622, France Abstract Wolbachia is one of the most abundant endosymbionts on earth, with a wide distribution especially in arthropods. Effective maternal transmission and the induction of various phenotypes in their hosts are two key features of this bacterium. Here, we review our current understanding of another central aspect of Wolbachia’s success: their ability to switch from one host species to another. We build on the proposal that Wolbachia host shifts occur in four main steps: 1) physical transfer to a new species, 2) proliferation within that host, 3) successful maternal transmission, and 4) spread within the host species. Host shift occasions can fail at each of these steps, and the likelihood of ultimate success is influenced by many factors. Some stem from Wolbachia properties (different strains have different abilities for host switching), others on host features such as genetic resemblance (e.g. host shifting is likely to be easier between closely related species), ecological connections (donor and recipient host need to interact with each other), or the resident microbiota. Host shifts have enabled Wolbachia to reach its enormous current incidence and global distribution among arthropods in an epidemiological process shaped by loss and acquisition events across host species. The ability of Wolbachia to transfer between species also forms the basis of ongoing endeavours to control pests and disease vectors, following artificial introduction into uninfected hosts such as mosquitoes. Throughout, we emphasise the many knowledge gaps in our understanding of Wolbachia host shifts, and question the effectiveness of current methodology to detect these events. We conclude by discussing an apparent paradox: how can Wolbachia maintain its ability to undergo host shifts given that its biology seems dominated by vertical transmission? Keywords: Ecological connection, endosymbiont, host switching, host shift steps, horizontal transmission, transmission route, epidemiology, phylogenetics 2 Table of Contents I. Introduction ..................................................................................................................... 4 II. Steps involved in host shifts ........................................................................................ 8 Step 1: Physical transfer .......................................................................................................... 8 Predator-prey interactions .................................................................................................................................. 9 Host-parasitoid/parasite interactions .......................................................................................................... 10 Shared plant and other food sources ............................................................................................................. 11 Step 2: Survival and proliferation in the new host ....................................................... 12 Step 3: Vertical transmission ............................................................................................... 15 Step 4: Spread within the host population ...................................................................... 16 III. Factors influencing host shifts ................................................................................ 19 3.1. Host resident microBiome ............................................................................................ 20 3.2. Host shift aBility of Wolbachia strains ...................................................................... 21 3.3. Genetic similarity of the donor and recipient hosts ............................................ 22 3.4. The role of ecology .......................................................................................................... 24 IV. Implications of Wolbachia host shifts .................................................................. 26 4.1. Host shifts and between-host epidemiological dynamics .................................. 26 4.2. Host shifts and their reciprocal effect on Wolbachia genetic diversity ......... 28 4.3. Applied aspects of Wolbachia host shifts ................................................................. 29 V. Outlook and open questions .................................................................................... 30 VI. Conclusions .................................................................................................................... 35 Acknowledgments ............................................................................................................... 36 References .............................................................................................................................. 36 3 I. Introduction The genus name Wolbachia denotes a diverse group of a-proteobacteria that live as maternally inherited endosymbionts in many arthropods and nematodes (Hertig, 1936; Sironi et al., 1995). During the last decades, these bacteria have received much attention from researchers and the general public for three main reasons. First, they induce a wide range of fascinating phenotypes in their hosts, often detrimental and with wide-ranging evolutionary consequences (Charlat et al., 2003; Werren et al., 2008; Engelstädter & Hurst, 2009). Second, Wolbachia is one of the most abundant symbionts, with around 50% of all arthropod species being infected (Hilgenboecker et al., 2008; Zug & Hammerstein, 2012; Weinert et al., 2015; Bailly-Bechet et al., 2017). Finally, Wolbachia can be adopted as a controlling agent against vector-borne pathogens such as dengue, as well as pest species (Kambris et al., 2009; Iturbe-Ormaetxe et al., 2011; Asgari, 2017; Ross et al., 2019) . The diversity of phenotypes induced by these bacteria include reproductive manipulations (Yen & Barr, 1971; Rousset et al., 1992; Hurst et al., 2000), physiological and behavioural modifications (Min & Benzer, 1997; Beltran-Bech & Richard, 2014; Rohrscheib et al., 2015; Truitt et al., 2018; Bi & Wang, 2020) and changes in their susceptibility to pathogens (Hedges et al., 2008; Teixeira et al., 2008; Kambris et al., 2009; Ekwudu et al., 2020). Wolbachia can also contribute to nutrient synthesis (e.g. Brownlie et al., 2009; Moriyama et al., 2015). Reproductive manipulations are common and take various forms. In cytoplasmic incompatibility (CI), Wolbachia induces embryonic death in the offspring of uninfected females mated with infected males. In the case of male killing, the bacteria cause the death of sons in the offspring of infected females. Finally, parthenogenesis and feminisation induction both stem from the transformation of potential males into females, which effectively leads to parthenogenesis in host species where zygotes can develop without mating. From an evolutionary standpoint, these various effects can all be explained as adaptations enhancing the bacteria’s fitness through that of the infected hosts, or more specifically the infected “matrilines”, that is, the Wolbachia-carrying cytoplasmic lineages (Cosmides & Tooby, 1981; Werren, 1997; Stouthamer et al., 1999). This reasoning is straightforward in the case of direct positive effects such as protection 4 against pathogens or nutrients provision, but possibly less so when it comes to reproductive manipulations, where maternal (as opposed to biparental) transmission is the critical feature (Werren et al., 2008). In the case of CI, the relative fitness of infected embryos is only indirectly increased by the elevated death in the offspring of uninfected females mated with infected males (Hoffmann et al., 1990; O’Neill et al., 1997). Male- killing also has indirect fitness consequences in the sense that the death of infected females’ sons does not immediately (and possibly not always) benefit their sisters: only reduced competition for food, or even consumption of their dead brothers, can generate some “fitness compensation” that will give an advantage to the infected cytoplasmic lineage (Hurst & Majerus, 1993). Finally, in species where Wolbachia induces parthenogenesis or feminisation, its benefits are most evident and strong: in both cases,