Reproductive Parasitism and Positive Fitness Effects of Heritable Microbes

Abstract

The classification of host–symbiont relationships is usually defined along the parasitism‐mutualism spectrum. It has long been proposed that transmission route is a key factor driving this, with vertical transmission leading to mutualism and horizontal transmission leading to parasitism. However, uniparental vertical transmission can lead to the evolution of reproductive parasitism, whereby host reproduction is skewed to increase the proportion of females within a population or else to reduce the comparative fitness of uninfected females (to the detriment of overall host fitness). Once discussed separately from beneficial effects and mutualism, we now recognise reproductive parasitism is not exclusive of other symbiont phenotypes. We outline the evolution and relationship of reproductive parasitism with respect to positive fitness effects for hosts, and how these interactions may be dynamic across the parasitism‐mutualism continuum. Key Concepts Exclusive maternal transmission of microbes can create strong selection for reproductive parasitism. Heritable microbes are also selected to confer a range of positive effects on host function and physiology. Where heritable microbes act both as reproductive parasites, and as a positive influence on host function, they are referred to as Jekyll and Hyde symbionts. The presence of positive effects on host function can facilitate the invasion and maintenance of reproductive parasites in host populations. Reproductive parasitism may likewise provide a context in which symbionts may evolve host‐beneficial phenotypes. Symbionts that combine reproductive parasitism with positive effects on host function constitute a useful mechanism for modification of insect host biology in natural populations, coupling a strong gene drive system to a beneficial trait. The presence of multiple phenotypes may aid the spread of heritable microbes through host communities, by enabling host shift events. Lateral transfer of genetic information between microbes can provide the mutational mechanism through which Jekyll and Hyde symbionts arise.

Rapid molecular evolution of Spiroplasma symbionts of Drosophila

“…In arthropods, such associations are the rule, and maternally inherited, endosymbiotic bacteria are especially common and diverse [2, 3]. Prominent examples include obligate nutritional symbionts of blood and sap feeders [4], reproductive manipulators [5], and protective symbionts [6]. Collectively, inherited symbionts of arthropods are highly diverse with respect to potential benefits and costs induced, and their degree of adaptation to hosts.…”

Rapid molecular evolution ofSpiroplasmasymbionts ofDrosophila

“…In arthropods, such associations are the rule, and maternally inherited, endosymbiotic bacteria are especially common and diverse (Duron et al, 2008;Weinert et al, 2015). Prominent examples include obligate nutritional symbionts of blood and sap feeders (Douglas, 2009), reproductive manipulators (Drew et al, 2019), and protective symbionts (Oliver et al, 2014). Collectively, inherited symbionts of arthropods are highly diverse with respect to potential benefits and costs induced, and their degree of adaptation to hosts.…”

Effects, interactions, and localization of Rickettsia and Wolbachia in the house fly parasitoid, Spalangia endius

“…These reproductive manipulations include the induction of parthenogenesis, male killing (male embryos die before hatching), feminization (genetic males develop as females), and cytoplasmic incompatibility (CI; a cross between a symbiont-infected male and an uninfected female is incompatible, thereby reducing the proportion of uninfected individuals in the population). Secondary symbionts are usually maternally transmitted, but horizontal transmission can occasionally occur as well [2][3][4][5]. To date, five bacterial genera are known as reproductive manipulators (also commonly termed reproductive parasites): Arsenophonus, Cardinium, Flavobacteria relatives, Rickettsia, Spiroplasma, and Amit Semiatizky and Benjamin Weiss contributed equally to this work.…”