Abstract

Metazoans host complex communities of microorganisms that include dinoflagellates, fungi, bacteria, archaea and viruses. Interactions among members of these complex assemblages allow hosts to adjust their physiology and metabolism to cope with environmental variation and occupy different habitats. Here, using reciprocal transplantation across depths, we studied adaptive divergence in the corals Orbicella annularis and O. franksi, two young species with contrasting vertical distribution in the Caribbean. When transplanted from deep to shallow, O. franksi experienced fast photoacclimation and low mortality, and maintained a consistent bacterial community. By contrast, O. annularis experienced high mortality and limited photoacclimation when transplanted from shallow to deep. The photophysiological collapse of O. annularis in the deep environment was associated with an increased microbiome variability and reduction of some bacterial taxa. Differences in the symbiotic algal community were more pronounced between coral species than between depths. Our study suggests that these sibling species are adapted to distinctive light environments partially driven by the algae photoacclimation capacity and the microbiome robustness, highlighting the importance of niche specialization in symbiotic corals for the maintenance of species diversity. Our findings have implications for the management of these threatened Caribbean corals and the effectiveness of coral reef restoration efforts.

Highlights

  • Understanding how microbial biodiversity interacts with their hosts’ physiology is essential for understanding animal ecology and evolution [1]

  • Across the vertical distribution range of each species, it is estimated that the light intensity varies between 18% and 62% sea surface irradiance for O. annularis and between 5% and 33% for O. franksi

  • We found a significant species by depth interaction (F1,102 = 28.78, p < 0.001), indicating that the slope of the regression model describing the relationship between Qm and depth was significantly different between species, being more than twice as pronounced in O. annularis (m = −0.13; R2 = 0.71, p < 0.001) than in O. franksi (m = −0.05; R2 = 0.50, p < 0.001)

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Summary

Introduction

Understanding how microbial biodiversity interacts with their hosts’ physiology is essential for understanding animal ecology and evolution [1]. Microbial communities often influence their hosts’ physiology to cope with environmental variation across habitats [2]. Reef-building corals (Cnidaria: Scleractinia) form a symbiotic association with dinoflagellates, which allow corals to thrive on the ocean’s euphotic zone along a strong depth-mediated light gradient [3]. Coral colonies at different depths may host distinctive symbiotic algae with contrasting photoacclimation capabilities that grant their hosts the ability to thrive in certain light environments [6,7]. Because of these differences in photoacclimation and the prevalence of specific associations with coral hosts, zonation by light has been regarded as a primary form of niche partitioning in symbiotic corals [8]

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