Spiders, microbes and sex: Bacterial exposure on copulatory organs alters mating behaviour in funnel‐web spiders

Abstract

Environmental microbes have the potential to be involved in nearly all behavioural processes. For example, mating systems where males use intromittent organs to transfer sperm to females represent a means by which environmental microbes collected by males can breach entry into females' body cavities during mating. However, the degree to which the acquisition of environmental microbes onto important sex structures alters courtship behaviours remains unknown. Here, we collected bacteria from the copulatory organs of Agelenopsis pennsylvanica funnel‐weaving spiders in situ to test whether exposure to bacteria on copulatory organs can alter hosts' courtship behaviour, reproductive success and survival. We used a standardized assay to repeatedly measure each spider's aggressiveness, a behavioural component of both male courtship and female sexual receptivity. Then, we experimentally altered the bacteria present on male and female spiders' copulatory organs with an application of either (a) a mixture of bacteria collected from conspecifics to increase bacterial presence, (b) an antibiotic to reduce bacterial presence or (c) a procedural control. Each spider was paired with a size‐matched spider of the opposite sex whose copulatory organs were unaltered, and we measured the latency until the onset and the duration of courtship. Spiders were then isolated, and we measured each individual's time until death and female fecundity over the next 40 days. We found that female exposure to bacteria had multiple effects on mating dynamics. Males took over four times longer to begin courting females that had been exposed to bacteria compared to unexposed and antibiotic‐treated females. Only when courting these bacteria‐exposed females, males began courtship sooner when females were more aggressive. Lastly, females whose mate had been exposed to bacteria experienced reduced survival. These data suggest that bacteria present on animals' copulatory organs can alter courtship behaviours, female survivorship, and may potentially play a role in mating dynamics.

The protamines of the noble false widow spiderSteatoda nobilisprovide an example of liquid-liquid phase separation chromatin transitions during spermiogenesis

“…This may be because, in contrast to previous studies, in the case of S. nobilis only the protein products present in the mature sperm obtained from the spider pedipalps were used in the analysis. The detection of bacterial protein/peptides in this study is consistent with this, as spiders like S. nobilis use intromittent organs to transfer sperm to females, and environmental microbes are introduced into females during mating (Spicer et al, 2019).…”

The Reproductive Microbiome: An Emerging Driver of Sexual Selection, Sexual Conflict, Mating Systems, and Reproductive Isolation

“…As we develop an understanding of the structural and functional diversity of reproductive microbiomes, more refined definitions may begin to emerge, with a narrower focus and more specialised to the biology of different systems. Such definitions might benefit from identifying the host and/or site of the microbiome (e.g., the human reproductive microbiome [7], the vaginal microbiome of primates [11], or the microbiome of copulatory organs of spiders [108]).…”

Parasites of spiders: Their impacts on host behavior and ecology

“…Those that engaged in reproductive activity exhibited a significant reduction in lytic activity. These results suggest a down-regulation of immunity associated with the expression of reproductive behaviors, which could leave spiders more susceptible to sexually-transmitted microbes (Spicer et al 2019). found that the ingestion of bacteria as a juvenile leads to stronger immune responses in adult S. ochreata wolf spiders, but was also associated with decreased body condition and asymmetrical foreleg tufts, which is an important sexually-selected trait.…”

“…It is unlikely that exposure to cuticular bacteria alone can induce these changes, but none of these studies identified the route by which bacteria enter the host body after a topical application. Spicer et al (2019) applied a cocktail of cuticular bacteria onto A. pennsylvanica sex organs, and found that females who mated with males whose pedipalps were exposed to bacteria experienced reduced survivorship compared to females who had bacteria injected directly into the epigynum. Thus, the epigynum may not represent a potential route for the acquisition of environmental microbes but transfer from male intromittent organs (the embolus) warrants further study.…”