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Eco-Evo-Devo: developmental symbiosis and developmental plasticity as evolutionary agents

Key Points

  • Developmental symbiosis and developmental plasticity contribute in numerous ways to animal evolution

  • Symbionts help to generate organs and maintain species-specific interactions with their animal hosts.

  • Symbionts provide selectable variation and can generate the conditions for reproductive isolation

  • Symbionts may have promoted major evolutionary transitions such as multicellularity

  • Plasticity allows the integration of the organism into its environment, changing development to account for predators, conspecifics, diet and temperature.

  • Plasticity provides the raw material for genetic accommodation and niche construction.

  • Plasticity can both help and harm populations experiencing stresses such as global climate change.

Abstract

The integration of research from developmental biology and ecology into evolutionary theory has given rise to a relatively new field, ecological evolutionary developmental biology (Eco-Evo-Devo). This field integrates and organizes concepts such as developmental symbiosis, developmental plasticity, genetic accommodation, extragenic inheritance and niche construction. This Review highlights the roles that developmental symbiosis and developmental plasticity have in evolution. Developmental symbiosis can generate particular organs, can produce selectable genetic variation for the entire animal, can provide mechanisms for reproductive isolation, and may have facilitated evolutionary transitions. Developmental plasticity is crucial for generating novel phenotypes, facilitating evolutionary transitions and altered ecosystem dynamics, and promoting adaptive variation through genetic accommodation and niche construction. In emphasizing such non-genomic mechanisms of selectable and heritable variation, Eco-Evo-Devo presents a new layer of evolutionary synthesis.

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Figure 1: Milestones towards a new vision for the central importance of symbiotic interactions as being fundamental to all aspects of animal biology.

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Acknowledgements

S.F.G. is supported by National Science Federation (NSF) grant IOS 145177 and by a Swarthmore College faculty research award. T.C.G.B. is supported by grants from the Deutsche Forschungsgemeinschaft (DFG) and by the DFG Cluster of Excellence Inflammation at Interfaces. C.L.R is supported by NSF grants IOS 1120209 and IOS 1256689.

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Glossary

Ecological evolutionary developmental biology

(Eco-Evo-Devo). The scientific programme that incorporates the rules governing the interactions between an organism's genes, development and environment into evolutionary theory.

Reproductive isolation

The phenomenon whereby members of two potentially interbreeding populations are prevented from producing viable or fertile hybrid offspring.

Holobionts

The eukaryotic organism (host) plus its persistent symbionts. The cow, for instance, is a combination of the mammalian body plus the symbionts, the enzymes of which allow it to digest grasses, and so on.

Microbiomes

The totality of microorganisms and their collective genetic material present in or on the body of a macroscopic host organism or in another environment.

Germ-free mice

Mice bred in sterile facilities with no contact with microorganisms.

Chemotaxis

The movement of an entity such as a cell along a gradient of chemical concentration towards the source of the chemical.

Gnotobiotic

A condition when the investigator knows all of the microorganisms in the host. Germ-free mice are often called gnotobiotic. Gnotobiotic animals are born in aseptic conditions and immediately transferred to an isolation area where all incoming air, food and water is sterilized.

Extragenetic inheritance

Mechanisms of inherited variation that are not derived from nucleic acid composition variants in the parent.

Epialleles

DNA sequences that are identical by nucleic acid composition but may differ in their secondary modifications such as DNA methylation, histone acetylation or methylation, or chromatin context. Also known as epimutations when they differ from wildtype.

Genotype-by-environment interactions

Processes wherein different genotypes respond to environmental variation in different ways.

Choanoflagellate

A group of unicellular and colonial flagellates that are thought to be the sister group of multicellular animals.

Genetic assimilation

A subset of genetic accommodation, whereby a trait induced by the environment becomes part of the genetic repertoire of the organism.

Bithorax

When the third thoracic segment of a fly becomes a repeat of the second thoracic segment, creating two sets of wings.

Polyphenism

The phenomenon when the same genotype can give rise to two or more distinct functional phenotypes.

Modern synthesis

Also called the neo-Darwin synthesis, this model of evolution reconciles natural selection with Mendelian genetics.

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Gilbert, S., Bosch, T. & Ledón-Rettig, C. Eco-Evo-Devo: developmental symbiosis and developmental plasticity as evolutionary agents. Nat Rev Genet 16, 611–622 (2015). https://doi.org/10.1038/nrg3982

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