Abstract

The widespread temporal and spatial persistence of endosymbionts in arthropod host populations, despite potential conflicts with their hosts and fluctuating environmental conditions, is puzzling. Here, we disentangled three main mechanisms that are commonly proposed to explain such persistence, namely, obligatory relationships, in which the host is fully dependent on its endosymbiont, fitness advantages conferred by the endosymbiont, and reproductive manipulations imposed by the endosymbiont. Our model system reflects an extreme case, in which the Wolbachia endosymbiont persists in all female flea hosts but rarely in male ones. We cured fleas of both sexes of Wolbachia but found no indications for either lower reproduction, offspring survival, or a change in the offspring sex ratio, compared to Wolbacia-infected fleas. These results do not support any of the suggested mechanisms. We highlight future directions to advance our understanding of endosymbiont persistence in fleas, as well as in other model systems, with extreme sex-differences in endosymbiont persistence. Insights from such studies are predicted to shed light on the evolution and ecology of arthropod-endosymbiont interactions in nature.

Highlights

  • Prevalent and dense endosymbiont populations that persist in arthropod host populations, despite potential conflicts with their hosts and fluctuating environmental conditions, are widespread in nature (Feldhaar, 2011)

  • The tetracycline supplementation worked efficiently, as even after three antibiotic-free generations, there was no indication of Wolbachia in any of the treated fleas that were tested (N = 88 parental females, N = 13 female offspring, and N = 20 parental males)

  • Consistent with the Wolbachia loads observed in wild fleas (Flatau et al, 2018), loads were significantly higher for control females than for control males (3 × 105 ± 2 × 105, for females, and 7 × 103 ± 1 × 104, for males)

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Summary

INTRODUCTION

Prevalent and dense endosymbiont populations that persist in arthropod host populations, despite potential conflicts with their hosts and fluctuating environmental conditions, are widespread in nature (Feldhaar, 2011). Wolbachia can spread and persist in the host population by manipulating their host’s reproduction to enhance the fitness of infected females. In natural populations, all female fleas in all sampling locations and times possess Wolbachia at high loads (3 × 105 ± 2 × 105), whereas from 0 to 54% of the males possess Wolbachia at a detectable level, with low infection loads (7 × 103 ± 1 × 104; Cohen et al, 2015; Flatau et al, 2018) Such extreme bias in the endosymbiont persistence pattern suggests that the two sexes are prone to divergent selection pressures (Richardson et al, 2019). Endosymbiont occurrence in the gut and gut appendages may suggest a nutritional role (Ben-Yosef et al, 2020; Reis et al, 2020)

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