Understanding cryptic coral diversity: A 3Dreefscape genomics approach to assess dispersal dynamics and niche differentiation

Abstract  Corals provide habitat for numerous marine species and ecosystem services for global human populations. However, they are vulnerable to local and global scale threats, especially climate change. Measuring demographic processes such as dispersal and ecological processes such as niche partitioning are important for predicting their responses to disturbances and environmental change. So far, correlations between coral genetics and the environment or spatial scale have largely been made over large habitat distinctions, such as depth, reef zone, and among islands or geographic regions. Reefs comprise structurally heterogenous landscapes and thus microhabitats may vary considerably, however, we have little understanding of how genotypes are distributed within reefs across fine spatial scales. Dynamics at fine spatial scales are particularly important in corals due to the frequent discovery of genetically divergent but morphologically indistinguishable coral taxa found sympatrically within reefs (i.e., cryptic taxa, often with no obvious environmental distinctions) and evidence that dispersal distances may be small for some taxa. Technological advancements in both genomic sequencing and underwater imaging and computation can help to study fine-scale dispersal and determine whether cryptic taxa are ecologically partitioned. Reduced representation sequencing can be conducted on wild populations and gives access to genomic variation across hundreds of individuals. Structure-from-motion photogrammetry enables the characterisation of structural features of the reef and coral colonies within reefs; thus, it is possible to combine high resolution spatial mapping and micro-environment analyses with genotyped colonies using these two technologies. 

Species of the Caribbean hard coral genus Agaricia (Order: Scleractinia) are arrayed over the entire depth range for photosynthetically dependent organisms, making them an ideal target for comparing mesophotic (>30 m depth) and shallow (<30 m) species, evaluating microhabitat differentiation, and assessing spatial structures across depths. My thesis uses this genus to explore questions related to spatial and environmental differentiation between and within taxa at scales from tens of kilometres to centimetres. The first data chapter (Chapter 2) of my thesis focuses on two mesophotic-occurring species: Agaricia grahamae and A. lamarcki. Despite presuming to be brooders with localised dispersal, no spatial population genetic structure was found over 10s of kms in either species. However, two sympatrically occurring cryptic taxa within each species were found. In A. lamarcki these taxa exhibited incomplete depth partitioning between shallow and mesophotic depths, yet taxa within A. grahamae displayed no obvious environmental distinctions. Demographic histories of all taxa were characterised by gene flow among taxa. This chapter exemplifies the complexities found in corals, where (1) spatial genetic structures do not follow expectations, (2) morphologically similar, sympatric taxa exist both at the same depths and differentiated by shallow and mesophotic depths and (3) gene flow among taxa may be important for the evolution of corals. My second and third data chapters (Chapters 3 and 4) focus on fine-scale characterisation of genotypes across 3D-imaged reefscapes within three depth zones (5, 10, 20 m) and among four sites along the leeward side of Curaçao and spread over ~50 km. Chapter 3 describes the delineation of cryptic coral taxa and investigates dispersal within and between depths among all taxa. The cryptic taxa are defined by divergent genotypic clusters occurring sympatrically and some were found to be associated with particular depth profiles. Disparate spatial genetic structures were found among congeners, where taxa within A. agaricites and A. humilis presented isolation-by-distance and dispersal distances across metres and, in contrast, A. lamarcki taxa presented genetic homogeneity at distances >50 km. This chapter provides one of the few estimates of dispersal distances in corals, which is exceedingly low (across metres), highlights the widespread cryptic diversity within corals and finds substantial differences in dispersal, clonality and genetic diversity among congeners. In Chapter 4, I used photogrammetry to characterise the microhabitat around individually genotyped colonies of Agaricia by deriving novel geometric measures. Environmental niches for sympatric cryptic taxa were determined by describing microhabitats that coral colonies inhabit. Species and cryptic taxa exhibited subtle divergences in their physical microhabitat niches. This chapter tackles the question of how cryptic coral taxa co-occur in seemingly similar environments and demonstrates a novel photogrammetric approach to characterise the microhabitat. 

My thesis applies new technologies and methods to help solve some of the mysteries of corals populations, namely, how far do larvae disperse? And what creates or preserves cryptic taxa? And in doing so, provides insight into coral ecology (interaction with microhabitat, spatial distribution, and dispersal) and evolution (cryptic diversification and hybridisation).