Multiple endosymbiont infections and reproductive manipulations in a linyphiid spider population

Abstract

In many arthropods, maternally inherited endosymbiotic bacteria can increase infection frequency by manipulating host reproduction. Multiple infections of different bacteria in a single host population are common, yet few studies have documented concurrent endosymbiont phenotypes or explored their potential interactions. We hypothesized that spiders might be a particularly useful taxon for investigating endosymbiont interactions, because they are host to a plethora of endosymbiotic bacteria and frequently exhibit multiple infections. We established two matrilines from the same population of the linyphiid spider Mermessus fradeorum and then used antibiotic curing and controlled mating assays to demonstrate that each matriline was subject to a distinct endosymbiotic reproductive manipulation. One matriline was co-infected with Rickettsia and Wolbachia and produced offspring with a radical female bias. Antibiotic treatment eliminated both endosymbionts and restored an even sex ratio to subsequent generations. Chromosomal and fecundity observations suggest a feminization mechanism. In the other matriline, a separate factorial mating assay of cured and infected spiders demonstrated strong cytoplasmic incompatibility (CI) induced by a different strain of Wolbachia. However, males with this Wolbachia induced only mild CI when mated with the Rickettsia-Wolbachia females. In a subsequent survey of a field population of M. fradeorum, we detected these same three endosymbionts infecting 55% of the spiders in almost all possible combinations, with nearly half of the infected spiders exhibiting multiple infection. Our results suggest that a dynamic network of endosymbionts may interact both within multiply infected hosts and within a population subject to multiple strong reproductive manipulations.

Insights into the bacterial symbiont diversity in spiders

“…Co-infection of multiple endosymbionts in the arthropods host was common (Duron et al, 2008;Engelstädter & Hurst, 2009;Goodacre et al, 2006), and relatively few studies have explored the phenotypic effect of multiple endosymbionts on their hosts (Curry, Paliulis, Welch, Harwood, & White, 2015;White, Kelly, Cockburn, Perlman, & Hunter, 2011). Little information has been obtained in relation to the emulative distribution of multiple endosymbionts in their hosts.…”

Hidden suppression of sex ratio distortion suggests Red queen dynamics between Wolbachia and its dwarf spider host

“…This lack of phenotypic differentiation between populations provides further evidence for the potentially hidden nature of suppressors, which is consistent with the hypothesis that endosymbionts and suppressors readily evolve in response to endosymbiont infection. At least for the Araneae order this could partly explain the discrepancy between the high number of spider species infected with endosymbionts (Goodacre et al, 2006) and the paucity of cases in which their effects have been demonstrated (Gunnarsson et al, 2009;Vanthournout et al, 2011Vanthournout et al, , 2014Curry et al, 2015) or are apparently absent (Stefanini & Duron, 2012). Moreover, endosymbiont infection is increasingly regarded as a major consideration in arthropod conservation biology (Nice et al, 2009).…”

“…Here, we explore whether endosymbiotic effects may be phenotypically hidden by the action of host suppressor genes in the dwarf spider Oedothorax gibbosus. Although spiders have been shown to be a particular hotspot for certain endosymbionts (Duron et al, 2008b), only a very limited number of studies have shown reproductive effects (Gunnarsson et al, 2009;Vanthournout et al, 2011Vanthournout et al, , 2014Curry et al, 2015). The dwarf spider Oedothorax gibbosus is infected with a male-killing Wolbachia that causes a similarly femalebiased sex ratio (Vanthournout et al, 2011).…”

Wolbachia Associations with Insects: Winning or Losing Against a Master Manipulator

“…Feminization induced by Wolbachia has been demonstrated in lepidopteran and hemipteran insects and spiders (Negri, 2012;Curry et al, 2015). In the butterfly Eurema hecabe, it has been demonstrated that the Wolbachia feminizing effect acts continuously throughout the larval development for the maintenance of the female phenotype (Narita et al, 2007).…”