A microbial perspective on the life‐history evolution of marine invertebrate larvae: If, where and when to feed

Abstract

The feeding environment for planktotrophic larvae has a major impact on development and progression towards competency for metamorphosis. High phytoplankton environments that promote growth and development also correlate with a greater abundance of environmental microbes and incidence of pathogenic microbes, making these habitats potentially risky for larvae. Trade‐offs between metabolic processes for growth and immune functionality have been described throughout the animal kingdom and may influence the life‐history evolution of marine invertebrate planktotrophic larvae. Specifically, larvae would be predicted to regulate time spent between these feeding environments to avoid potential incidences of microbial‐mediated mortality and/or dysbiosis. Using transcriptomic and microbiome data, we provide evidence for this trade‐off in larvae of the sea urchin Strongylocentrotus droebachiensis. When cultured in a well‐fed environment, larvae upregulate genes associated with metabolism while decreasing the expression of genes associated with immune function. At the same time, the associated bacterial community shifts towards a state of dysbiosis that is followed by mortality. To test whether the environmental microbiota is a selective force on if, where and when planktotrophic larvae should feed, we conclude by presenting a strategy for determining the specific interactions of larvae and microbes at a scale representative of their pelagic environment.

Bacterial Exposure Mediates Developmental Plasticity and Resistance to Lethal Vibrio lentus Infection in Purple Sea Urchin (Strongylocentrotus purpuratus) Larvae

“…However, feeding-associated plasticity typically manifests as reduced gut size and increased arm length relative to body length under low food conditions, and our low bacterial load (P/S) animals were larger in all measurements (body length, gut area, post-oral arm length, anterolateral arm length) besides the body rod, which is not typically plastic in response to food (83). One explanation is that bacterial exposure mediates a trade-off between growth and immune competence during development, as predicted in Carrier et al (82). In this model, larvae expend energy to establish and maintain a molecular and/or cellular immune state that would otherwise be diverted to growth and development in the absence of bacteria.…”

“…In this study, we found that the sizes of multiple larval structures were associated with differences in bacterial exposure during development. At first glance, this effect appeared similar to feeding-associated phenotypic plasticity, as planktotrophic larvae consume bacteria, and gut bacteria are associated with digestive and metabolic functions in countless taxa (2,3,7,8), including larval (38,82) and adult sea urchins (27,69). However, feeding-associated plasticity typically manifests as reduced gut size and increased arm length relative to body length under low food conditions, and our low bacterial load (P/S) animals were larger in all measurements (body length, gut area, post-oral arm length, anterolateral arm length) besides the body rod, which is not typically plastic in response to food (83).…”

Symbiotic Life of Echinoderm Larvae

“…It has since been observed that additional planktotrophic echinoderms exhibit bacterivory and that this feeding mode is hypothesized to be important, but not essential, to the metabolic requirements of the larva (Pearse et al, 1991;Douillet, 1993;Ayukai, 1994;Moal et al, 1996;Gosselin and Qian, 1997). Based on maximum clearance rates and particle abundance, it is estimated that echinoderm larvae interact with ∼20 million bacteria each day by feeding alone (Carrier et al, 2018a). It is, however, unknown which bacterial (or other microbial) groups that echinoderm larvae may target and whether these microbes are selected strictly for bacterivory or as a symbiont that may be acquired by horizontal transmission.…”

“…Less of this work, however, has focused on embryonic and larval echinoderms. Echinoderm larvae potentially interact with ∼20 million bacteria each day by feeding alone (Carrier et al, 2018a), and a portion of these bacteria may be consumed through bacterivory, be symbionts acquired by horizontal transmission, or pathogenic bacteria that require an immune response.…”

“…When faced with variation in food quantity, larval echinoids exhibit a trade-off in the expression of immune and metabolic genes (Carrier et al, 2015(Carrier et al, , 2018a, such that well-fed larvae upregulate metabolism and suppress immunity. High food availability is also suitable environmental conditions for bacteria to express pathogenic characteristics.…”