Defining Coral Bleaching as a Microbial Dysbiosis within the Coral Holobiont.

Coral microbiomes are critical to holobiont health and functioning, but the stability of host-microbial interactions is fragile, easily shifting from eubiosis to dysbiosis. The heat-induced breakdown of the symbiosis between the host and its dinoflagellate algae (that is, "bleaching"), is one of the most devastating outcomes for reef ecosystems. Yet, bleaching tolerance has been observed in some coral species. This review provides an overview of the holobiont's diversity, explores coral thermal tolerance in relation to their associated microorganisms, discusses the hypothesis of adaptive dysbiosis as a mechanism of environmental adaptation, mentions potential solutions to mitigate bleaching, and suggests new research avenues. More specifically, we define coral bleaching as the succession of three holobiont stages, where the microbiota can (i) maintain essential functions for holobiont homeostasis during stress and/or (ii) act as a buffer to mitigate bleaching by favoring the recruitment of thermally tolerant Symbiodiniaceae species (adaptive dysbiosis), and where (iii) environmental stressors exceed the buffering capacity of both microbial and dinoflagellate partners leading to coral death.

Parentage analyses identify local dispersal events and sibling aggregations in a natural population of Millepora hydrocorals, a free-spawning marine invertebrate.

Dispersal is a critical process for the persistence and productivity of marine populations. For many reef species, there is increasing evidence that local demography and self-recruitment have major consequences on their genetic diversity and adaptation to environmental change. Yet empirical data of dispersal patterns in reef-building species remain scarce. Here, we document the first genetic estimates of self-recruitment and dispersal distances in a free-spawning marine invertebrate, the hydrocoral Millepora cf. platyphylla. Using twelve microsatellite markers, we gathered genotypic information from 3,160 georeferenced colonies collected over 27,000 m2 of a single reef in three adjacent habitats in Moorea, French Polynesia; the mid slope, upper slope, and back reef. Although the adult population was predominantly clonal (85% were clones), our parentage analysis revealed a moderate self-recruitment rate with a minimum of 8% of sexual propagules produced locally. Assigned offspring often settled at <10 m from their parents and dispersal events decrease with increasing geographic distance. There were no discrepancies between the dispersal distances of offspring assigned to parents belonging to clonal versus nonclonal genotypes. Interhabitat dispersal events via cross-reef transport were also detected for sexual and asexual propagules. Sibship analysis showed that full siblings recruit nearby on the reef (more than 40% settled at <30 m), resulting in sibling aggregations. Our findings highlight the importance of self-recruitment together with clonality in stabilizing population dynamics, which may ultimately enhance local sustainability and resilience to disturbance.

Historical changes (1905-present) in catch size and composition reflect altering fisheries practices on a small Caribbean island.

Effective assessments of the status of Caribbean fish communities require historical baselines to adequately understand how much fish communities have changed through time. To identify such changes and their causes, we compiled a historical overview using data collected at the beginning (1905-1908), middle (1958-1965) and end (1984-2016) of the 20th century, of the artisanal fishing practices and their effects on fish populations around Curaçao, a small island in the southern Caribbean. We documented historical trends in total catch, species composition, and catch sizes per fisher per month for different types of fisheries and related these to technological and environmental changes affecting the island's fisheries and fish communities. We found that since 1905, fishers targeted species increasingly farther from shore after species occurring closer to shore had become rare. This resulted in surprisingly similar catches in terms of weight, but not composition. Large predatory reef fishes living close to shore (e.g., large Epinephelid species) had virtually disappeared from catches around the mid-20th century, questioning the use of data from this period as baseline data for modern day fish assessments. Secondly, we compared fish landings to in-situ counts from 1969 to estimate the relative contributions of habitat destruction and overfishing to the changes in fish abundance around Curaçao. The decline in coral dominated reef communities corresponded to a concurrent decrease in the abundance and diversity of smaller reef fish species not targeted by fishers, suggesting habitat loss, in addition to fishing, caused the observed declines in reef fish abundance around Curaçao.

On the occurrence of intracolonial genotypic variability in highly clonal populations of the hydrocoral Millepora platyphylla at Moorea (French Polynesia).

Intracolonial genotypic variability is described in many colonial organisms and arises from mosaicism (somatic mutation) and/or chimerism (allogenic fusion). Both processes provide an additional source of genotypic variation in natural populations and raise questions on the biological significance of colonies having more than one genotype. Using fifteen microsatellite markers, we screened for potential genetic heterogeneity within Millepora platyphylla colonies, a hydrocoral species known for its extensive morphological plasticity among reef habitats. We aimed to determine whether mosaicism and chimerism were related to specific reef habitats and/or colony morphologies. Our results show that intracolonial genotypic variability was common (31.4%) in M. platyphylla at Moorea, French Polynesia, with important variations in its frequency among habitats (0-60%), while no effect of morphology was observed. Mosaicism seemed responsible for most of the genetic heterogeneity (87.5%), while chimerism was rarer. Some mosaics were shared among fire coral clones indicating that mutations could be spread via colony fragmentation. Further, the genotypic variability among clones suggests that colonies produced asexually through fragmentation have the potential to accumulate their own mutations over time. Such mutation dynamics might have important implications for the adaptive potential of long-lived reef-builder populations that are predominantly sustained through asexual reproduction.

Fire coral clones demonstrate phenotypic plasticity among reef habitats.

Clonal populations are often characterized by reduced levels of genotypic diversity, which can translate into lower numbers of functional phenotypes, both of which impede adaptation. Study of partially clonal animals enables examination of the environmental settings under which clonal reproduction is favoured. Here, we gathered genotypic and phenotypic information from 3,651 georeferenced colonies of the fire coral Millepora platyphylla in five habitats with different hydrodynamic regimes in Moorea, French Polynesia. In the upper slope where waves break, most colonies grew as vertical sheets ("sheet tree") making them more vulnerable to fragmentation. Nearly all fire corals in the other habitats are encrusting or massive. The M. platyphylla population is highly clonal (80% of the colonies are clones), while characterized by the highest genotype diversity ever documented for terrestrial or marine populations (1,064 genotypes). The proportion of clones varies greatly among habitats (≥58%-97%) and clones (328 clonal lineages) are distributed perpendicularly from the reef crest, perfectly aligned with wave energy. There are six clonal lineages with clones dispersed in at least two adjacent habitats that strongly demonstrate phenotypic plasticity. Eighty per cent of the colonies in these lineages are "sheet tree" on the upper slope, while 80%-100% are encrusting or massive on the mid slope and back reef. This is a unique example of phenotypic plasticity among reef-building coral clones as corals typically have wave-tolerant growth forms in high-energy reef areas.

Genetic diversity and differentiation in reef-building Millepora species, as revealed by cross-species amplification of fifteen novel microsatellite loci.

Quantifying the genetic diversity in natural populations is crucial to address ecological and evolutionary questions. Despite recent advances in whole-genome sequencing, microsatellite markers have remained one of the most powerful tools for a myriad of population genetic approaches. Here, we used the 454 sequencing technique to develop microsatellite loci in the fire coral Millepora platyphylla, an important reef-builder of Indo-Pacific reefs. We tested the cross-species amplification of these loci in five other species of the genus Millepora and analysed its success in correlation with the genetic distances between species using mitochondrial 16S sequences. We succeeded in discovering fifteen microsatellite loci in our target species M. platyphylla, among which twelve were polymorphic with 2-13 alleles and a mean observed heterozygosity of 0.411. Cross-species amplification in the five other Millepora species revealed a high probability of amplification success (71%) and polymorphism (59%) of the loci. Our results show no evidence of decreased heterozygosity with increasing genetic distance. However, only one locus enabled measures of genetic diversity in the Caribbean species M. complanata due to high proportions of null alleles for most of the microsatellites. This result indicates that our novel markers may only be useful for the Indo-Pacific species of Millepora. Measures of genetic diversity revealed significant linkage disequilibrium, moderate levels of observed heterozygosity (0.323-0.496) and heterozygote deficiencies for the Indo-Pacific species. The accessibility to new polymorphic microsatellite markers for hydrozoan Millepora species creates new opportunities for future research on processes driving the complexity of their colonisation success on many Indo-Pacific reefs.

Population structure of the hydrocoral Millepora platyphylla in habitats experiencing different flow regimes in Moorea, French Polynesia.

While the fire coral Millepora platyphylla is an important component of Indo-Pacific reefs, where it thrives in a wide range of environments, the ecological and biological processes driving its distribution and population structure are not well understood. Here, we quantified this species' population structure in five habitats with contrasting hydrodynamic regimes in Moorea, French Polynesia; two in the fore reef: mid and upper slopes, and three in the lagoon: back, fringing and patch reefs. A total of 3651 colonies of fire corals were mapped and measured over 45,000 m2 of surveyed reef. Due to the species' sensitivity to fragmentation in response to strong water movement, hydrodynamic conditions (e.g. waves, pass and lagoonal circulation) corresponded to marked differences in colony size distributions, morphology and recruitment dynamics among habitats. The size structure varied among reef habitats with higher proportions of larger colonies in calm nearshore reefs (fringing and patch reefs), while populations were dominated by smaller colonies in the exposed fore reefs. The highest densities of fire corals were recorded in fore reef habitats (0.12-0.20 n.m-2) where the proportion of recruits and juveniles was higher at mid slope populations (49.3%) than on the upper slope near where waves break (29.0%). In the latter habitat, most colonies grew as vertical sheets on encrusting bases making them more vulnerable to colony fragmentation, whereas fire corals were encrusting or massive in all other habitats. The lowest densities of M. platyphylla occurred in lagoonal habitats (0.02-0.04 n.m-2) characterized by a combination of low water movement and other physical and biological stressors. This study reports the first evidence of population structure of fire corals in two common reef environments and illustrates the importance of water flow in driving population dynamic processes of these reef-building species.