The Octocorallia represent a group of globally distributed colonial marine invertebrates with species represented from intertidal to abyssal depths. With a predicted Precambrian origin, octocorals are an ancient lineage with a long evolutionary history. During this time they have differentiated into genetically diverse taxa that exhibit a broad range of colonial morphologies, including a variety of branched forms.
This PhD focuses on evolutionary processes responsible for producing extant diversity in octocoral habitat, genotype and phenotype. At the level of genotype, I examine the origins of a novel mitochondrial gene and its putative functional role in octocoral evolution. At the level of phenotype, I reconstruct the phylogenetic patterns and evolutionary dynamics of convergent colonial growth forms within a globally distributed family of octocorals. Finally, in this same family I study the patterns of depth range shifts in ancestral lineages that are responsible for a broad modern bathymetric distribution and determine the main depth regions responsible for the production of extant biodiversity.
The mtMutS gene is only found in the mitochondrial genomes of octocorals, where it has been proposed to have a role in DNA mismatch repair. Although octocorals display relatively low rates of mitochondrial divergence, an analysis of the potential for this gene to be functional has not been attempted. In addition, previous phylogenetic analyses of the bacterial MutS and eukaryotic MSH gene families have suggested that mtMutS may have originated via horizontal gene transfer from a microbial ancestral source into the octocorallian common ancestor. I confirm an exogenous origin of mtMutS using a comprehensive phylogenetic reconstruction. Furthermore, using gene expression analysis and bioinformatic prediction of protein function and structure, I demonstrate that, across a diverse range of octocorals, mtMutS is expressed and the predicted protein product displays the necessary functional constraints and domain architecture for a self-sufficient role in DNA repair. A comparative analysis of rates of mitochondrial evolution between octocorals and the Hexacorallia indicates that the former displays significantly reduced levels of genetic divergence, consistent with a hypothesis of functional mtMutS activity within the mitochondria.
Using DNA sequences of mtMutS as a molecular marker, I next explore the systematic relationships and evolutionary dynamics underpinning morphological diversity of the Ellisellidae. This octocoral family displays a series of increasingly branched colonial growth patterns ranging from unbranched whips through to highly ramified and anastomosing net-like fans. The Ellisellidae is bisected according to sclerite forms and is then divided into genera on the basis of branching form. My phylogenetic results indicate that six of eight morphologically-defined genera are polyphyletic due to biogeographical incompatibilities and are in need of taxonomic revision. Ancestral reconstruction of branching morphology predicts an identical ordered progression, or parallelism, in each of the two primary lineages of ellisellids, providing support for the existence of constraints on the genetic mechanisms determining colonial morphology. Although further study is suggested, a lack of correspondence between levels of genetic divergence and morphological diversity between genera suggests that modifications to the regulatory control of branching genes may be responsible for evolutionary changes in branching morphology.
I conclude with an analysis of ancestral patterns of depth range changes in the Ellisellidae, which are found from upper euphotic to lower mesophotic zones. The genera of this family display partitioning among depth zones but an understanding of the genesis of this variation in depth range is lacking for this family and many other sessile invertebrates with varied vertical ranges. I use a combination of divergence time estimation and two corroborative methods of reconstructing ancestral depth ranges to determine the rate and directionality of bathymetric shifts in the evolution of the Ellisellidae. A mesophotic Cretaceous common ancestor is predicted, with subsequent Paleogene divergences producing gradual emergent and submergent evolutionary trends, corresponding to each of two primary lineages. A secondary emergence occurs in the Neogene, producing further euphotic diversity with expansion of two genera into the Atlantic. The multiple mesophotic origins of extant euphotic taxa indicate an evolutionary role of deeper environments in producing shallow-water biodiversity. Although it appears that bathymetric shifts may only be fast enough to act in the recovery, rather than the resilience, of associated benthic habitats, further investigation is needed into the factors driving changes in rates of depth expansions over various timescales.
In summary, the research conducted during the course of this PhD 1) provides evidence of evolutionary constraint underlying diversity and convergence of colonial branching morphologies, 2) identifies an evolutionary role of mesophotic depth zones in originating shallow-water diversity in an exemplary group of octocorals and 3) demonstrates that an exogenously acquired mtMutS gene displays a form and activity consistent with a role in mitochondrial DNA repair. These findings provide a foundation for future genomic research into the evolutionary role of the nuclear genome in generating morphological diversity and variation in habitat selectivity and the role of microbial associations in ancient metazoan evolution.