Developmental symbiosis facilitates the multiple origins of herbivory

Abstract

Developmental bias toward particular evolutionary trajectories can be facilitated through symbiosis. Organisms are holobionts, consisting of zygotederived cells and a consortia of microbes, and the development, physiology, and immunity of animals are properties of complex interactions between the zygotederived cells and microbial symbionts. Such symbionts can be agents of developmental plasticity, allowing an organism to develop in particular directions. This plasticity can lead to genetic assimilation either through the incorporation of microbial genes into host genomes or through the direct maternal transmission of the microbes. Such plasticity can lead to niche construction, enabling the microbes to remodel host anatomy and/or physiology. In this article, I will focus on the ability of symbionts to bias development toward the evolution of herbivory. I will posit that the behavioral and morphological manifestations of herbivorous phenotypes must be preceded by the successful establishment of a community of symbiotic microbes that can digest cell walls and detoxify plant poisons. The ability of holobionts to digest plant materials can range from being a plastic trait, dependent on the transient incorporation of environmental microbes, to becoming a heritable trait of the holobiont organism, transmitted through the maternal propagation of symbionts or their genes. K E Y W O R D S

Evolutionary transitions revisited: Holobiont evo‐devo

“…Here, the progression through a particular stage of the life cycle is mediated by chemicals or contacts with sessile micro‐organisms (Freckelton, Nedved, & Hadfield, ). However, such life‐cycle regulation is also readily seen in ruminant vertebrates (Gilbert, ). The cow, for instance, has no genes that would enable it to digest the cellulose, hemicellulose, and pectins that are so abundant in the grass she eats.…”

“…However, such life-cycle regulation is also readily seen in ruminant vertebrates (Gilbert, 2019). The cow, for instance, has no genes that would enable it to digest the cellulose, hemicellulose, and pectins that are so abundant in the grass she eats.…”

Historical and philosophical perspectives on the study of developmental bias

“…(Gilbert, 2019) form the basis for biases in phenotypic variation. Many will argue that an explanation of developmental bias requires more than the study of gene regulatory mechanisms.…”

“…Although the idea of a developmental mechanism's variational properties is an empirically adequate notion, it again includes any instance of variation. Examples of developmental biases due to symbiosis likewise broaden the scope of a general explanatory framework that can include metabolic and physiological interactions between organisms of different species (Gilbert, 2019). Moreover, in addition to simply indicating that there is some evolutionary issue worthy of study, in Section 3 I emphasized that that an agenda-setting concept plays a substantial coordinating function to the extent to which it also encompasses criteria of explanatory adequacy, which guide research by indicating what an explanatory framework must include and what shape it has to take.…”

Biases in the study of developmental bias

“…Laland et al (2019) explore the different types of biases that may manifest along the way, and when and how they may affect adaptive evolution, evolutionary rates and outcomes, and evolvability. Another major evolutionary transition is the subject of a contribution by Gilbert (2019), namely the role of developmental symbioses in the multiple origins of herbivory. Here, the term "domestication syndrome" refers to a suite of behavioral, morphological, and physiological traits that all underwent concerted evolutionary change during domestication events, even though none of them were selected deliberately, thereby providing a particularly compelling example of developmental bias in evolution.…”