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In mesophotic coral ecosystems, reef-building corals and their photosynthetic symbionts can survive with less than 1% of surface irradiance. How depth-specialist corals rely upon autotrophically and heterotrophically derived energy sources across the mesophotic zone remains unclear. We analysed the stable carbon (δ¹³C) and nitrogen (δ¹⁵N) isotope values of aLeptoseriscommunity from the ‘Au‘au Channel, Maui, Hawai‘i (65–125 m) including four coral host species living symbiotically with three algal haplotypes. We characterized the isotope values of hosts and symbionts across species and depth to compare trophic strategies. Symbiontδ¹³C was consistently 0.5‰ higher than hostδ¹³C at all depths. Mean colony host and symbiontδ¹⁵N differed by up to 3.7‰ at shallow depths and converged at deeper depths. These results suggest that both heterotrophy and autotrophy remained integral to colony survival across depth. The increasing similarity between host and symbiontδ¹⁵N at deeper depths suggests that nitrogen is more efficiently shared between mesophotic coral hosts and their algal symbionts to sustain autotrophy. Isotopic trends across depth did not generally vary by host species or algal haplotype, suggesting that photosynthesis remains essential toLeptoserissurvival and growth despite low light availability in the mesophotic zone.

 

Coevolution—reciprocal evolutionary change between interacting lineages (Thompson, 1994; see Glossary)—is thought to have played a profound role in the evolution of Life on Earth. From similar patterns across the wings of unrelated lineages of butterflies (Hoyal Cuthill and Charleston, 2015), egg mimicry of “cheating” brood parasites (Davies, 2010), to the role of animal pollinators in driving the diversification of flowering plants (Kay and Sargent, 2009), to the ubiquity of sexual reproduction and sexual conflicts (Hamilton, 2002; Arnqvist and Rowe, 2005; King et al., 2009), the formation of the eukaryotic cell (Martin et al., 2015; Imachi et al., 2020), and even the origin of living organisms themselves (Mizuuchi and Ichihashi, 2018), evolutionary changes among interacting lineages have played profound and important roles in the history of Life. This Grand Challenges inaugural contribution encompasses eclectic opinions of the editorial board as to what are the next frontiers of coevolution research in the 21st century. Coevolutionary biology is a field that has garnered a lot of attention in recent years, in part as a result of technical advances in nucleotide sequencing and bioinformatics in the burgeoning field of host–microbial interactions. Many seminal studies of coevolution examined reciprocal evolutionary change between two or a few interacting macroscopic species that imposed selective pressures on one another (e.g., insect or bird pollinators and their flowering host plants). Understanding the contexts under which coevolution occurs, as opposed to scenarios in which each partner adapts independently to a particular environment (Darwin, 1862; Stiles, 1978) is important to elucidate coevolutionary processes. A whole spectrum of organismal interactions has been examined under the lens of coevolution, providing additional context, and nuance to ecological strategies traditionally categorized as ranging from beneficial to detrimental for participating species (Figure 1). In particular, a coevolutionary perspective has revealed that even “mutualisms” are not always fully beneficial or cooperative for the partners involved. Instead, the tendency to “cheat” permeates across symbiotic partnerships (Perez-Lamarque et al., 2020). Conversely, recent evidence suggests that non-lethal predation by co-evolved predators, which has traditionally been assumed to be entirely antagonistic, may provide sessile prey with some indirect benefit through enhanced opportunities to acquire beneficial symbiotic microorganisms (Grupstra et al., 2021). Herein, we discuss some of the recent areas of active research in coevolution, restricting our focus to coevolution between interacting species. 

Mesophotic reef corals remain largely unexplored in terms of the genetic adaptations and physiological mechanisms to acquire, allocate, and use energy for survival and reproduction. In the Hawaiian Archipelago, theLeptoserisspecies complex form the most spatially extensive mesophotic coral ecosystem known and provide habitat for a unique community. To study how the ecophysiology ofLeptoserisspecies relates to symbiont–host specialization and understand the mechanisms responsible for coral energy acquisition in extreme low light environments, we examinedSymbiodinium(endosymbiotic dinoflagellate) photobiological characteristics and the lipids and isotopic signatures fromSymbiodiniumand coral hosts over a depth‐dependent light gradient (55–7μmol photons m⁻²s⁻¹, 60–132 m). Clear performance differences demonstrate different photoadaptation and photoacclimatization across this genus. Our results also show that flexibility in photoacclimatization depends primarily onSymbiodiniumtype. Colonies harboringSymbiodiniumsp.COI‐2showed significant increases in photosynthetic pigment content with increasing depth, whereas colonies harboringSymbiodiniumspp.COI‐1andCOI‐3showed variability in pigment composition, yield measurements for photosystem II, as well as size and density ofSymbiodiniumcells. Despite remarkable differences in photosynthetic adaptive strategies, there were no significant differences among lipids ofLeptoserisspecies with depth. Finally, isotopic signatures of both host andSymbiodiniumchanged with depth, indicating that coral colonies acquired energy from different sources depending on depth. This study highlights the complexity in physiological adaptations within this symbiosis and the different strategies used by closely related mesophotic species to diversify energy acquisition and to successfully establish and compete in extreme light‐limited environments.