Evolutionary and ecological connectivity at hierarchical scales from sperm to species in the reef-building coral genus Seriatopora

Determining the spatial scales of ecological connectivity for marine populations, which typically exist as metapopulations of spatially isolated subpopulations linked by demographic processes (e.g., larval dispersal, reproduction), is critical for foundational taxa, yet poorly understood for the reef-building corals. Connectivity of populations on ecological timescales is becoming increasingly relevant to conservation and management efforts, as the pace of changing climate and anthropogenic impacts accelerates and the need to understand processes sustaining the resilience of coral populations becomes more urgent. In this thesis, I investigated three hierarchical divisions (species, populations and individuals) within the coral genus Seriatopora to resolve spatial scales of genetic linkages and elucidate the ecological and evolutionary processes that determine connectivity in the group, and interpret these results in light of population recovery and resilience. To determine if cryptic diversity occurs in the abundant coral morphospecies Seriatopora hystrix, as suggested by inconsistent results from reproductive, population genetics and recent mitochondrial studies, multiple lines of evidence (genetic, ecological and morphological) were combined to compare diversity within S. hystrix to that found between S. hystrix and its only known congener on the Great Barrier Reef (GBR), Seriatopora caliendrum (Chapter 2). Based on hierarchical Bayesian clustering of microsatellite data, four distinct clusters were identified within S. hystrix that demonstrate genetic cohesion across two regions of the GBR separated by 450 km in both sympatric and allopatric populations. Correlations between mtDNA phylotypes, combined with habitat preference, Symbiodinium spp. coupling and in one case, morphology, corroborate these clusters as putative cryptic species. Moreover, the four putative cryptic species are diverged from each other at levels comparable to genetic differentiation at microsatellite loci from S. caliendrum (F(ST): 0.337 – 0.519). Only one instance of recent hybridization was inferred between the morphospecies S. hystrix and S. caliendrum, but none were detected among the putative cryptic species of S. hystrix. One rare putative species, only sampled in one region (Sh_bushy), displays a distinctive morphology and is almost fixed for private alleles (>82%) at one of the ten loci. Moreover, a phylogeographic analysis of all published Seriatopora mitochondrial control region sequences revealed clear affinities among some proximate geographic regions (e.g., GBR and New Caledonia) and one cosmopolitan lineage that occurs in five of eight locations surveyed from Okinawa to the GBR. Together, these findings suggest that species diversity within the genus Seriatopora is higher than expected on the GBR, and imply that global diversity may also be higher for the genus, both of which have significant implications for our ability to accurately assess and conserve biodiversity, and infer connectivity patterns. Using the putative cryptic species identified in Chapter 2 as separate units, I determined and compared levels of population connectivity for the two most abundant putative species, which respectively dominate sheltered (leeward) and exposed (windward) habitats, at three hierarchical spatial scales on the GBR: within reefs (<1 km), between reefs (<10 km), and among regions (~450 km) (Chapter 3). Standard equilibrium population differentiation statistics were combined with Bayesian clustering and spatial autocorrelation analyses, using ten microsatellite loci and individual-level geographic coordinates from seventeen populations. I found consistent patterns of genetic subdivision among reefs and regions, in contrast to previous work, suggesting that widespread cryptic species in S. hystrix may account for some of the complex genetic structure previously reported. Significantly, I determined that mean larval dispersal is concentrated within 3 km of source populations for both putative species, indicating that local recovery from disturbances in these putative species will likely be dependent on relatively close proximity of surviving populations. Recolonization following local extinctions in isolated areas may be possible, but much less certain on immediate time scales. Within a population, sperm dispersal constitutes the mechanism by which brooding sessile corals interact and mate, and forms the first link in the network of processes that determine species-wide genetic diversity and connectivity patterns, but almost nothing is known about sperm dispersal for any internally fertilizing coral. I conducted a parentage analysis on brooded coral larvae collected from a mapped population to measure the distance of sperm dispersal for the first time in a reef-building coral, and to estimate mating system characteristics of the putative Seriatopora species that dominates sheltered habitats (Chapter 4). Furthermore, I define and apply consensus criteria among several replicated methods to maximize accuracy in paternal assignments for a natural population. Thirteen progeny arrays indicated that this putative species produces sexually derived, primarily outcrossed larvae (mean t(m)=0.999 ±0.026 SD) in multiple paternity broods (mean r(p)=0.119 ±0.052 SD). Self-fertilization was directly detected only at very low frequency for all broods combined (2.8%), but comprised 23% of matings in one brood. Although over 82% of mating occurred between colonies within 10 m of each other (mean sperm dispersal = 5.5 m ±4.37 SD), I found no evidence of inbreeding in the genetic structure of the established population. In particular, more limited dispersal of sperm, compared to greater distances of philopatric larval dispersal, appears to reduce inbreeding among close relatives in this cryptic species. Given mounting evidence that a diverse range of coral reef organisms exhibit restricted dispersal and potentially widespread cryptic species, protected area networks must be designed with the appropriate criteria in mind, particularly in relation to the size, spacing and inclusion of diverse habitats, to maintain demographic, ecological and evolutionary processes. The results of my research indicate that species diversity may be much higher than previously thought for the genus Seriatopora, an abundant and geographically widespread group of corals. Ecological distributions imply specific habitat preferences for the two dominant putative species, for which the majority of larval dispersal appears to be limited to very local areas (<3 km). However, high population densities and frequent reproductive events throughout the year suggest local resilience and imply that local populations can be successfully preserved. Moreover, the absence of inbreeding, despite relatively small genetic neighborhoods, indicates that mechanisms exist to promote and preserve genetic diversity within populations of these species. Taken together, my results indicate that local conservation efforts will constitute an important strategy for long-term persistence of the genus, and, providing that environmental integrity can be maintained, connectivity processes will continue to support abundant populations of this important group of corals over broad spatial scales.