Mark J. A. Vermeij

Abstract

Multicellularity evolved multiple times independently during eukaryotic diversification. Two distinct mechanisms underpin multicellularity: clonal development (serial cell division of a
single precursor cell) and aggregation (in which independent cells assemble into a multicellular entity). Clonal and aggregative development are traditionally considered to be mutually exclusive and to result from independent acquisitions of multicellularity. Here, we show that the choanoflagellate Choanoeca flexa, a close relative of animals that forms contractile monolayers of cells (or “sheet colonies”), develops by an unconventional intermediate mechanism that we name “clonal-aggregative multicellularity”. We find that C. flexa sheets can form through purely clonal processes, purely aggregative processes, or a combination of both, depending on experimental conditions. To assess the ecological relevance of these findings, we characterize the natural context of multicellular development in the native environment of C. flexa on the island of Curaçao. We show that the C. flexa life cycle is environmentally regulated by extreme salinity fluctuations in splash pools undergoing cycles of evaporation and refilling. Upon desiccation, C. flexa colonies dissociate into drought resistant quiescent cells, which resume activity and reform multicellular sheets after rehydration. We hypothesize that clonal-aggregative development reflects selection for fast transitions into and out of multicellularity in the ephemeral context of coastal splash pools. Our findings underscore the potential of the exploration of biodiversity for revealing new fundamental biological phenomena and expand the known option space for both multicellular development and for the origin of animal multicellularity.

Theory suggests that the direct transmission of beneficial endosymbionts (mutualists) from parents to offspring (vertical transmission) in animal hosts is advantageous and evolutionarily stable, yet many host species instead acquire their symbionts from the environment (horizontal acquisition). An outstanding question in marine biology is why some scleractinian corals do not provision their eggs and larvae with the endosymbiotic dinoflagellates that are necessary for a juvenile's ultimate survival. We tested whether the acquisition of photosynthetic endosymbionts (family Symbiodiniaceae) during the planktonic larval stage was advantageous, as is widely assumed, in the ecologically important and threatened Caribbean reef-building coral Orbicella faveolata. Following larval acquisition, similar changes occurred in host energetic lipid use and gene expression regardless of whether their symbionts were photosynthesizing, suggesting the symbionts did not provide the energetic benefit characteristic of the mutualism in adults. Larvae that acquired photosymbionts isolated from conspecific adults on their natal reef exhibited a reduction in swimming, which may interfere with their ability to find suitable settlement substrate, and also a decrease in survival. Larvae exposed to two cultured algal species did not exhibit differences in survival, but decreased their swimming activity in response to one species. We conclude that acquiring photosymbionts during the larval stage confers no advantages and can in fact be disadvantageous to this coral host. The timing of symbiont acquisition appears to be a critical component of a host's life history strategy and overall reproductive fitness, and this timing itself appears to be under selective pressure.

Coral reef communities are often studied by tracking the percentage (or fraction) of the reef covered by coral through time. However, coral community dynamics result, in part, from underlying colony-level growth and mortality, which in turn depend on characteristics of individ- ual colonies, such as size, taxon, life history strategy, and morphology. Colonies are also subject to external disturbances that propel fission into smaller coral fragments and fusion where related fragments later fuse into contiguous colonies. To quantify how changes in coral growth through time depend on individual colony characteristics and colony fission and fusion processes, 4385 individual Caribbean coral colonies representing 4 dominant coral types (Madracis mirabilis, mounding coral species, Agaricia agaricites, and Millepora spp.) were tracked at 6 mo intervals for 4 yr. Despite overall stable percent coral cover, colonies belonging to different coral types experi- enced differential growth, shrinkage, mortality, fission, and fusion processes. All coral types dis- played size-dependent allometric growth patterns whereby relative, or proportional, growth in colony area decreased with increasing colony size. The largest changes in relative colony growth resulted from colony fission or fusion with other colonies, which occurred in 16.4% of all moni- tored colonies. Colony longevity, or survival, increased significantly with increasing colony size for all hard-coral groups that did not experience fission, fusion, or a combination of these pro- cesses. Our findings illustrate the usefulness of a size- and life-history-dependent approach to coral demography that elucidates the factors driving community dynamics of colonial organisms, which are not captured by traditional approaches based on benthic cover alone.

Apicomplexa is a group of obligate intracellular parasites that includes the causative agents of human diseases such as malaria and toxoplasmosis. Apicomplexans evolved from free-living phototrophic ancestors, but how this transition to parasitism occurred remains unknown. One potential clue lies in coral reefs, of which environmental DNA surveys have uncovered several lineages of uncharacterized basally branching apicomplexans. Reef-building corals have a well-studied symbiotic relationship with photosynthetic Symbiodiniaceae dinoflagellates (for example, Symbiodinium³), but the identification of other key microbial symbionts of corals has proven to be challenging. Here we use community surveys, genomics and microscopy analyses to identify an apicomplexan lineage—which we informally name ‘corallicolids’—that was found at a high prevalence (over 80% of samples, 70% of genera) across all major groups of corals. Corallicolids were the second most abundant coral-associated microeukaryotes after the Symbiodiniaceae, and are therefore core members of the coral microbiome. In situ fluorescence and electron microscopy confirmed that corallicolids live intracellularly within the tissues of the coral gastric cavity, and that they possess apicomplexan ultrastructural features. We sequenced the genome of the corallicolid plastid, which lacked all genes for photosystem proteins; this indicates that corallicolids probably contain a non-photosynthetic plastid (an apicoplast). However, the corallicolid plastid differs from all other known apicoplasts because it retains the four ancestral genes that are involved in chlorophyll biosynthesis. Corallicolids thus share characteristics with both their parasitic and their free-living relatives, which suggests that they are evolutionary intermediates and implies the existence of a unique biochemistry during the transition from phototrophy to parasitism.

One mechanism giving fleshy algae a competitive advantage over corals during reef degradation is algal-induced and microbially-mediated hypoxia (typically less than 69.5 µmol oxygen L⁻¹). During hypoxic conditions oxygen availability becomes insufficient to sustain aerobic respiration in most metazoans. Algae are more tolerant of low oxygen conditions and may outcompete corals weakened by hypoxia. A key question on the ecological importance of this mechanism remains unanswered: How extensive are local hypoxic zones in highly turbulent aquatic environments, continuously flushed by currents and wave surge? To better understand the concert of biological, chemical, and physical factors that determine the abundance and distribution of oxygen in this environment, we combined 3D imagery, flow measurements, macro- and micro-organismal abundance estimates, and experimentally determined biogenic oxygen and carbon fluxes as input values for a 3D bio-physical model. The model was first developed and verified for controlled flume experiments containing coral and algal colonies in direct interaction. We then developed a three-dimensional numerical model of an existing coral reef plot off the coast of Curaçao where oxygen concentrations for comparison were collected in a small-scale grid using fiberoptic oxygen optodes. Oxygen distribution patterns given by the model were a good predictor for in situ concentrations and indicate widespread localized differences exceeding 50 µmol L^-1 over distances less than a decimeter. This suggests that small-scale hypoxic zones can persist for an extended period of time in the turbulent environment of a wave- and surge- exposed coral reef. This work highlights how the combination of three-dimensional imagery, biogenic fluxes, and fluid dynamic modeling can provide a powerful tool to illustrate and predict the distribution of analytes (e.g., oxygen or other bioactive substances) in a highly complex system.

Larval settlement in wave-dominated, nearshore environments is the most critical life stage for a vast array of marine invertebrates, yet it is poorly understood and virtually impossible to observe in situ. Using a custom-built flume tank that mimics the oscillatory fluid flow over a shallow coral reef, we show that millimeter-scale benthic topography increases the settlement of slow-swimming coral larvae by an order of magnitude relative to flat substrates. Particle tracking velocimetry of flow fields revealed that millimeter-scale ridges introduced regions of flow recirculation that redirected larvae toward the substrate surface and decreased the local fluid speed, effectively increasing the window of time for larvae to settle. In agreement with experiments, computational fluid dynamics modeling and agent-based larval simulations also showed significantly higher settlement on ridged substrates. These findings highlight how physics-based substrate design can create new opportunities to increase larval recruitment for ecosystem restoration.

ABSTRACT: The widespread loss of stony reef-building coral populations has been compounded by the low settlement and survival of coral juveniles. To rebuild coral communities, restoration practitioners have developed workflows to settle vulnerable coral larvae in the laboratory and outplant settled juveniles back to natural and artificial reefs. These workflows often make use of natural biochemical settlement cues, which are presented to swimming larvae to induce settlement. This paper establishes the potential for inorganic cues to complement these known biochemical effects. Settlement substrates were fabricated from calcium carbonate, a material present naturally on reefs, and modified with additives including sands, glasses, and alkaline earth carbonates. Experiments with larvae of two Caribbean coral species revealed additive-specific settlement preferences that were independent of bulk surface properties such as mean roughness and wettability. Instead, analyses of the substrates suggest that settling coral larvae can detect localized topographical features more than an order of magnitude smaller than their body width and can sense and positively respond to soluble inorganic minerals such as silica (SiO2) and strontianite (SrCO3). These findings open a new area of research in coral reef restoration, in which composite substrates can be designed with a combination of natural organic and inorganic additives to increase larval settlement and perhaps also improve post-settlement growth, mineralization, and defense.

Assisted gene flow (AGF) is a conservation intervention to accelerate
species adaptation to climate change by importing genetic
diversity into at-risk populations. Corals exemplify both the need for
AGF and its technical challenges; corals have declined in abundance,
suffered pervasive reproductive failures, and struggled to adapt to
climate change, yet mature corals cannot be easily moved for breeding,
and coral gametes lose viability within hours. Here, we report
the successful demonstration of AGF in corals using cryopreserved
sperm that was frozen for 2 to 10 y. We fertilized Acropora palmata
eggs from the western Caribbean (Curaçao) with cryopreserved
sperm from genetically distinct populations in the eastern and central
Caribbean (Florida and Puerto Rico, respectively). We then confirmed
interpopulation parentage in the Curaçao–Florida offspring
using 19,696 single-nucleotide polymorphism markers. Thus, we
provide evidence of reproductive compatibility of a Caribbean coral
across a recognized barrier to gene flow. The 6-mo survival of AGF
offspring was 42%, the highest ever achieved in this species, yielding
the largest wildlife population ever raised from cryopreserved
material. By breeding a critically endangered coral across its range
withoutmoving adults, we show that AGF using cryopreservation is
a viable conservation tool to increase genetic diversity in threatened
marine populations.

Abstract

A paramount challenge in coral reef ecology is to estimate the abundance and composition of the communities residing in such complex ecosystems. Traditional 2D projected surface cover estimates neglect the 3D structure of reefs and reef organisms, overlook communities residing in cryptic reef habitats (e.g., overhangs, cavities), and thus may fail to represent biomass estimates needed to assess trophic ecology and reef function. Here, we surveyed the 3D surface cover, biovolume, and biomass (i.e., ash-free dry weight) of all major benthic taxa on 12 coral reef stations on the island of Curaçao (Southern Caribbean) using structure-from-motion photogrammetry, coral point counts, in situ measurements, and elemental analysis. We then compared our 3D benthic community estimates to corresponding estimates of traditional 2D projected surface cover to explore the differences in benthic community composition using different metrics. Overall, 2D cover was dominated (52 ± 2%, mean ± SE) by non-calcifying phototrophs (macroalgae, turf algae, benthic cyanobacterial mats), but their contribution to total reef biomass was minor (3.2 ± 0.6%). In contrast, coral cover (32 ± 2%) more closely resembled coral biomass (27 ± 6%). The relative contribution of erect organisms, such as gorgonians and massive sponges, to 2D cover was twofold and 11-fold lower, respectively, than their contribution to reef biomass. Cryptic surface area (3.3 ± 0.2 m2 m−2planar reef) comprised half of the total reef substrate, rendering two thirds of coralline algae and almost all encrusting sponges (99.8%) undetected in traditional assessments. Yet, encrusting sponges dominated reef biomass (35 ± 18%). Based on our quantification of exposed and cryptic reef communities using different metrics, we suggest adjustments to current monitoring approaches and highlight ramifications for evaluating the ecological contributions of different taxa to overall reef function. To this end, our metric conversions can complement other benthic assessments to generate non-invasive estimates of the biovolume, biomass, and elemental composition (i.e., standing stocks of organic carbon and nitrogen) of Caribbean coral reef communities.