On the Spread of Microbes That Manipulate Reproduction in Marine Invertebrates

AbstractBacterial symbionts are functionally integral to animal reproduction and development, some of which have evolved additional mechanisms to override these host programs. One habitat that is increasingly recognized to contain phylogenetically related lineages of reproductive manipulators is the ocean. The reproduction of marine invertebrates often occurs by free spawning instead of by the physical contact of copulation in terrestrial systems. We developed an integrated model to understand whether and when microbes that manipulate host reproduction by cytoplasmic incompatibility, feminization, and male killing spread within populations of free-spawning marine invertebrates. Our model supports three primary findings. First, sex ratio distortion leads to suboptimal fertilization and zygote production in planktotrophs (feeding larvae) but enhance these processes in lecithotrophs (nonfeeding larvae). Second, feminization and a combination of male killing plus enhanced growth are effective at spreading reproductive manipulators while also inducing a female-biased sex ratio. Third, the majority of free-spawning marine invertebrates could be infected across a range of life history combinations, with infections harming species with smaller eggs and longer pelagic durations while benefiting species with larger eggs and shorter pelagic durations. Together, this supports the general premise that microbes may manipulate the reproduction of free-spawning marine invertebrates (e.g., by inducing changes in developmental life history) and that these types of manipulations overlap considerably with terrestrial systems.