Space and the persistence of male–killing endosymbionts in insect populations

Abstract

Male-killing bacteria are bacteria that are transmitted vertically through the females of their insect hosts. They can distort the sex ratio of their hosts by killing infected male offspring. In nature, male-killing endosymbionts (male killers) often have a 100% efficient vertical transmission, and multiple male-killing bacteria infecting a single population are observed. We use different model formalisms to study these observations. In mean-field models a male killer with perfect transmission drives the host population to extinction, and coexistence between multiple male killers within one population is impossible; however, in spatially explicit models, both phenomena are readily observed. We show how the spatial pattern formation underlies these results. In the case of high transmission efficiencies, waves with a high density of male killers alternate with waves of mainly wild-type hosts. The male killers cause local extinction, but this creates an opportunity for uninfected hosts to re-invade these areas. Spatial pattern formation also creates an opportunity for two male killers to coexist within one population: different strains create spatial regions that are qualitatively different; these areas then serve as different niches, making coexistence possible.

Evolution of early male-killing in horizontally transmitted parasites

“…R. Soc. B 282: 20152068 efficacy and a benefit provided to the surviving host offspring by killing the infected male embryos [10], and may also depend on their spatial distribution [11]. We showed that a purely vertically transmitted non-MK bacterium, otherwise able to invade the host as a highly efficient male-killer (electronic supplementary material, appendix S3), cannot persist and evolve MK gradually unless at least a bit of HT is present.…”

“…In fact, the presence of HT in MK bacteria could explain the existence of perfectly vertically transmitted male-killers in the field [24]. In spatial models, a perfectly vertically transmitted male-killer can both invade and persist in a host [11]. In the absence of any spatial component, the male-killer drives the population to extinction [10,25,26].…”

“…While we present them here only briefly, all are discussed at large in the electronic supplementary material, appendix S2. Given the VT efficacy j, the fitness benefit r conferred to the surviving offspring is expressed as [10,11] …”

Male-killing endosymbionts: influence of environmental conditions on persistence of host metapopulation

“…The only study [28] that explicitly addressed the persistence of male killing endosymbionts and infection prevalence within a spatial setting confirmed the importance of colonization-extinction dynamics, although at the local scale (i.e. within in a population).…”

Multi-Scale Modeling of Tissues Using CompuCell3D

“…The GGH has been continuously and successfully applied to model biological and biomedical processes, including Tumor growth (Dormann et al , 2001; dos Reis et al , 2003; Drasdo et al , 2003; Holm et al , 1991; Turner and Sherratt, 2002), Gastrulation (Drasdo and Forgacs, 2000; Drasdo et al , 1995; Longo et al , 2004), Skin pigmentation (Collier et al , 1996; Honda et al , 2002; Wearing et al , 2000), Neurospheres (Zhdanov and Kasemo, 2004a,b), Angiogenesis (Ambrosi et al , 2004; Ambrosi et al , 2005; Gamba et al ., 2003; Merks et al ., 2008; Merks and Glazier, 2006; Murray, 2003; Pierce et al ., 2004; Serini et al ., 2003), the Immune system (Kesmir and de Boer, 2003; Meyer-Hermann et al ., 2001), Yeast colony growth (Nguyen et al ., 2004; Walther et al ., 2004), Myxobacteria (Alber et al ., 2006; Arlotti et al ., 2004; Börner et al ., 2002; Bussemaker et al ., 1997; Dormann et al ., 2001), Stem cell differentiation (Knewitz and Mombach, 2006; Zhdanov and Kasemo, 2004a,b), Dictyostelium discoideum (Marée and Hogeweg, 2001, 2002; Marée et al ., 1999a,b; Savill and Hogeweg, 1997), Simulated evolution (Groenenboom and Hogeweg, 2002; Groenenboom et al ., 2005; Hogeweg, 2000; Johnston, 1998; Kesmir et al ., 2003; Pagie and Mochizuki, 2002), General developmental patterning (Honda and Mochizuki, 2002; Zhang et al , 2011), Convergent extension (Zajac, 2002; Zajac et al , 2002; Zajac et al ., 2003), Epidermal formation (Savill and Sherratt, 2003) Hydra regeneration (Mombach et al ., 2001; Rieu et al ., 2000), Plant growth , (Grieneisen et al ., 2007), Retinal patterning (Mochizuki, 2002; Takesue et al , 1998), Wound healing (Dallon et al , 2000; Maini et al ., 2002; Savill and Sherratt, 2003), Biofilms (Kreft et al ., 2001; Picioreanu et al ., 2001; Poplawski et al ., 2008; Van Loosdrecht et al ., 2002), Limb bud development (Chaturvedi et al ., 2004; Poplawski et al ., 2007), somite segmentation (Glazier et al ., 2008; Hester et al , 2011), vascular system development (Merks and Glazier, 2006), choroidal neovascularization, lumen formation, cellular intercalation (Zajac et al ., 2000, 2003), etc. ….…”