Abstract

BackgroundDivergent natural selection across environmental gradients has been acknowledged as a major driver of population and species divergence, however its role in the diversification of scleractinian corals remains poorly understood. Recently, it was demonstrated that the brooding coral Seriatopora hystrix and its algal endosymbionts (Symbiodinium) are genetically partitioned across reef environments (0-30 m) on the far northern Great Barrier Reef. Here, we explore the potential mechanisms underlying this differentiation and assess the stability of host-symbiont associations through a reciprocal transplantation experiment across habitats ('Back Reef', 'Upper Slope' and 'Deep Slope'), in combination with molecular (mtDNA and ITS2-DGGE) and photo-physiological analyses (respirometry and HPLC).ResultsThe highest survival rates were observed for native transplants (measured 14 months after transplantation), indicating differential selective pressures between habitats. Host-symbiont assemblages remained stable during the experimental duration, demonstrating that the ability to "shuffle" or "switch" symbionts is restricted in S. hystrix. Photo-physiological differences were observed between transplants originating from the shallow and deep habitats, with indirect evidence of an increased heterotrophic capacity in native deep-water transplants (from the 'Deep Slope' habitat). Similar photo-acclimatisation potential was observed between transplants originating from the two shallow habitats ('Back Reef' and 'Upper Slope'), highlighting that their genetic segregation over depth may be due to other, non-photo-physiological traits under selection.ConclusionsThis study confirms that the observed habitat partitioning of S. hystrix (and associated Symbiodinium) is reflective of adaptive divergence along a depth gradient. Gene flow appears to be reduced due to divergent selection, highlighting the potential role of ecological mechanisms, in addition to physical dispersal barriers, in the diversification of scleractinian corals and their associated Symbiodinium.

Highlights

  • Divergent natural selection across environmental gradients has been acknowledged as a major driver of population and species divergence, its role in the diversification of scleractinian corals remains poorly understood

  • We observed differential survival of ecotypes across habitats, no recombination between host and symbiont genotypes after transplantation, and photo-physiological differences between shallow and deep S. hystrix ecotypes. These observations confirm that the partitioning of these highly coupled host-symbiont associations across reef habitats reflects a process of adaptive divergence that is likely to be driven by environmental divergent selection

  • Divergent selection appears to have acted on the taxonomic unit of the coral holobiont, leading to adaptive divergence of host-symbiont pairs across reef habitats

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Summary

Introduction

Divergent natural selection across environmental gradients has been acknowledged as a major driver of population and species divergence, its role in the diversification of scleractinian corals remains poorly understood. The mechanisms that regulate and sustain diversity in both tropical rainforests and coral reefs remain heavily debated, it is clear that the characteristic environmental heterogeneity of these ecosystems must play an integral role by providing important axes for niche. Ecological adaptation through divergent selection can contribute to genetic divergence of populations (i.e., adaptive divergence), when the strength of selection overcomes the homogenizing effect of gene flow and recombination [12]. Rather than post-zygotic reproductive barriers, such as intrinsic hybrid sterility and genomic incompatibilities, gene flow between populations can be hampered through pleiotropic effects of selection [14]. It is unclear to what extent ecologically-based divergent selection, which should be ubiquitous on coral reefs given their environmental heterogeneity, contributes to the establishment of reproductive barriers in scleractinian corals

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