Microbes as manipulators of egg size and developmental evolution.

Abstract

Marine invertebrates mainly reproduce by energy-poor eggs that develop into feeding larvae or energy-rich eggs that develop into non-feeding larvae. Evolutionary transitions between these developmental modes have been studied in detail, yet the evolutionary factor(s) responsible for these switches remains elusive. Here, we use theoretical models to support the premise that microbes with the capacity to manipulate host reproduction may be one possible factor. Our model predicts that microbial manipulators could create a sperm-limited environment that selects for larger eggs by shifting the host's sex ratio toward female dominance and, as a result, drive an evolutionary transition in the developmental mode for marine invertebrates. The loss of a microbial manipulator could then recover the ancestral egg size and developmental mode. We also suggest more than a dozen genera of marine invertebrates from throughout the world's oceans that fit the framework of a microbe-induced evolutionary transition between these predominant developmental modes. We anticipate that microbial manipulators have a yet-to-be-appreciated influence on the developmental evolution of marine invertebrates. We find it paramount to understand whether evolutionary transitions in developmental mode occur with and without microbial manipulators as well as whether the underlying mechanisms of these manipulations are convergent with terrestrial systems.

Importance: Microbes that manipulate animal reproduction are widespread on land, and their evolutionary influence is widely acknowledged. Relatives of these manipulators are increasingly found in the ocean, but uniquely with taxa that recently underwent a transition in developmental evolution from feeding to non-feeding larvae. Here, we present theoretical models supporting that microbial manipulators could create a sperm-limited environment that selects for larger eggs by shifting the host's sex ratio toward female dominance and, as a result, drive an evolutionary transition in the developmental mode for free-spawning marine invertebrates. This theoretical model provides a complementary viewpoint to the theory regarding the evolutionary process that marine invertebrates undergo to transition between developmental modes as well as a fruitful opportunity to compare with terrestrial systems.