Domestication via the commensal pathway in a fish-invertebrate mutualism

Abstract

Domesticator-domesticate relationships are specialized mutualisms where one species provides multigenerational support to another in exchange for a resource or service, and through which both partners gain an advantage over individuals outside the relationship. While this ecological innovation has profoundly reshaped the world’s landscapes and biodiversity, the ecological circumstances that facilitate domestication remain uncertain. Here, we show that longfin damselfish (Stegastes diencaeus) aggressively defend algae farms on which they feed, and this protective refuge selects a domesticator-domesticate relationship with planktonic mysid shrimps (Mysidium integrum). Mysids passively excrete nutrients onto farms, which is associated with enriched algal composition, and damselfish that host mysids exhibit better body condition compared to those without. Our results suggest that the refuge damselfish create as a byproduct of algal tending and the mutual habituation that damselfish and mysids exhibit towards one another were instrumental in subsequent mysid domestication. These results are consistent with domestication via the commensal pathway, by which many common examples of animal domestication are hypothesized to have evolved.

Phylogeny of the Damselfishes (Pomacentridae) and Patterns of Asymmetrical Diversification in Body Size and Feeding Ecology

“…The Cheiloprionini likely evolved farming once with 4 losses, the Pomacentrinae 3 group twice in Hemiglyphidodon and Neoglyphidodon , and up to 6 origins in the Pomacentrinae (or two origins with multiple losses). Cultivating and defending an algal patch has long been recognized as an unusual level of behavioral complexity in fish feeding behavior (42,102,103), the intricacy of which recently increased as it has been shown to include the domestication of mysid shrimps by damselfishes to help fertilize the garden (104). All damselfish farmers are benthic, yet most benthic feeders are not farmers, and there is no significant character association between farming presence/absence and dietary ecotype across the phylogeny.…”

Long term relationship between farming damselfish, predators, competitors and benthic habitat on coral reefs of Moorea Island

“…Across the world’s coral reefs, some herbivorous fish are keystone species and the diverse array of species within this guild provides various ecosystem services, including those that may aid in the recovery of live hard coral 11 , 14 – 17 . By contrast, other keystone species, such as farming damselfish, can favor the development of algal turfs and defend them against other herbivorous fish 18 – 20 .…”

“…Reliance on algae for sustenance varies across Stegastes species, spanning from facultative to obligate 21 – 23 . They actively control the algal species composition within their farms, and defend them against other herbivorous fish, invertebrate micro-herbivorous grazers and sea-urchins 17 , 19 , 20 . In order to provide substratum for their algal field, they can actively removed scleractinian corals, such as by biting the living tissue and cultivating dense algal lawns on the coral skeletons 24 .…”

Human protection drives the emergence of a new coping style in animals

“…The generality of this concept, and its associated ecological and evolutionary consequences, will become clear only if the underlying genetic basis is understood. All the recent findings suggesting a link between protection from predators, and the emergence of a new coping style leaves another open question: whether this also occurs when domesticator-domesticate relationships involve other nonhuman species since such specific commensalisms exist in the wild [76]. We hope that future studies will allow us to better describe the conditions and the dynamics of the processes that favor the emergence of preactive individuals and help us understand the underlying mechanisms of these changes.…”