Early post-settlement events, rather than settlement, drive recruitment and coral recovery at Moorea, French Polynesia.

Understanding population dynamics is a long-standing objective of ecology, but the need for progress in this area has become urgent. For coral reefs, achieving this objective is impeded by a lack of information on settlement versus post-settlement events in determining recruitment and population size. Declines in coral abundance are often inferred to be associated with reduced densities of recruits, which could arise from mechanisms occurring at larval settlement, or throughout post-settlement stages. This study uses annual measurements from 2008 to 2021 of coral cover, the density of coral settlers (S), the density of small corals (SC), and environmental conditions, to evaluate the roles of settlement versus post-settlement events in determining rates of coral recruitment and changes in coral cover at Moorea, French Polynesia. Coral cover, S, SC, and the SC:S ratio (a proxy for post-settlement success), and environmental conditions, were used in generalized additive models (GAMs) to show that: (a) coral cover was more strongly related to SC and SC:S than S, and (b) SC:S was highest when preceded by cool seawater, low concentrations of Chlorophyll a, and low flow speeds, and S showed evidence of declining with elevated temperature. Together, these results suggest that changes in coral cover in Moorea are more strongly influenced by post-settlement events than settlement. The key to understanding coral community resilience may lie in elucidating the factors attenuating the bottleneck between settlers and small corals.

Larval and Adult Traits Coevolve in Response to Asymmetric Coastal Currents to Shape Marine Dispersal Kernels.

AbstractDispersal emerges as an outcome of organismal traits and external forcings. However, it remains unclear how the emergent dispersal kernel evolves as a by-product of selection on the underlying traits. This question is particularly compelling in coastal marine systems, where dispersal is tied to development and reproduction and where directional currents bias larval dispersal downstream, causing selection for retention. We modeled the dynamics of a metapopulation along a finite coastline using an integral projection model and adaptive dynamics to understand how asymmetric coastal currents influence the evolution of larval (pelagic larval duration) and adult (spawning frequency) life history traits, which indirectly shape the evolution of marine dispersal kernels. Selection induced by alongshore currents favors the release of larvae over multiple time periods, allowing long pelagic larval durations and long-distance dispersal to be maintained in marine life cycles in situations where they were previously predicted to be selected against. Two evolutionarily stable strategies emerged: one with a long pelagic larval duration and many spawning events, resulting in a dispersal kernel with a larger mean and variance, and another with a short pelagic larval duration and few spawning events, resulting in a dispersal kernel with a smaller mean and variance. Our theory shows how coastal ocean flows are important agents of selection that can generate multiple, often co-occurring evolutionary outcomes for marine life history traits that affect dispersal.

Hidden heatwaves and severe coral bleaching linked to mesoscale eddies and thermocline dynamics.

The severity of marine heatwaves (MHWs) that are increasingly impacting ocean ecosystems, including vulnerable coral reefs, has primarily been assessed using remotely sensed sea-surface temperatures (SSTs), without information relevant to heating across ecosystem depths. Here, using a rare combination of SST, high-resolution in-situ temperatures, and sea level anomalies observed over 15 years near Moorea, French Polynesia, we document subsurface MHWs that have been paradoxical in comparison to SST metrics and associated with unexpected coral bleaching across depths. Variations in the depth range and severity of MHWs was driven by mesoscale (10s to 100s of km) eddies that altered sea levels and thermocline depths and decreased (2007, 2017 and 2019) or increased (2012, 2015, 2016) internal-wave cooling. Pronounced eddy-induced reductions in internal waves during early 2019 contributed to a prolonged subsurface MHW and unexpectedly severe coral bleaching, with subsequent mortality offsetting almost a decade of coral recovery. Variability in mesoscale eddy fields, and thus thermocline depths, is expected to increase with climate change, which, along with strengthening and deepening stratification, could increase the occurrence of subsurface MHWs over ecosystems historically insulated from surface ocean heating by the cooling effects of internal waves.

Dispersal, kin aggregation, and the fitness consequences of not spreading sibling larvae.

Dispersal has far-reaching implications for individuals, populations, and communities, especially in sessile organisms. Escaping competition with conspecifics and with kin are theorized to be key factors leading to dispersal as an adaptation. However, manipulative approaches in systems in which adults are sessile but offspring have behaviors is required for a more complete understanding of how competition affects dispersal. Here, we integrate a series of experiments to study how dispersal affects the density and relatedness of neighbors, and how the density and relatedness of neighbors in turn affects fitness. In a marine bryozoan, we empirically estimated dispersal kernels and found that most larvae settled within ~1 m of the maternal colony, although some could potentially travel at least 10s of meters. Larvae neither actively preferred or avoided conspecifics or kin at settlement. We experimentally determined the effects of spreading sibling larvae by manipulating the density and relatedness of settlers and measuring components of fitness in the field. We found that settler density reduced maternal fitness when settler neighbors were siblings compared with when neighbors were unrelated or absent. Genetic markers also identified very few half sibs (and no full sibs) in adults from the natural population, and rarely close enough to directly interact. In this system, dispersal occurs over short distances (meters) yet, in contrast with expectations, there appears to be limited kinship between adult neighbors. Our results suggest that the limited dispersal increases early offspring mortality when siblings settle next to each other, rather than next to unrelated conspecifics, potentially reducing kinship in adult populations. High offspring production and multiple paternity could further dilute kinship at settlement and reduce selection for dispersal beyond the scale of 10s of meters.

Pocillopora tuahiniensis: a new species of scleractinian coral (Scleractinia, Pocilloporidae) from French Polynesia.

Pocillopora tuahiniensis sp. nov. is described based on mitochondrial and nuclear genomic data, algal symbiont genetic data, geographic isolation, and its distribution pattern within reefs that is distinct from other sympatric Pocillopora species (Johnston et al. 2022a, b). Mitochondrial and nuclear genomic data reveal that P. tuahiniensis sp. nov. is a unique species, sister to P. verrucosa, and in a clade different from that of P. meandrina (Johnston et al. 2022a). However, the gross in situ colony appearance of P. tuahiniensis sp. nov. cannot easily be differentiated from that of P. verrucosa or P. meandrina at Moorea. By sequencing the mtORF region, P. tuahiniensis sp. nov. can be easily distinguished from other Pocillopora species. Pocillopora tuahiniensis sp. nov. has so far been sampled in French Polynesia, Ducie Island, and Rapa Nui (Armstrong et al. 2023; Edmunds et al. 2016; Forsman et al. 2013; Glin et al. 2017; Mayfield et al. 2015; Oury et al. 2021; Voolstra et al. 2023). On the fore reefs of Moorea, P. tuahiniensis sp. nov. is very abundant 10 m and is one of the most common Pocillopora species at these depths (Johnston et al. 2022b). It can also be found at a much lower abundance at shallow depths on the fore reef and back reef lagoon. The holotype is deposited at the Smithsonian Institution as USNM-SI 1522390 and the mtORF Genbank accession number is OP418359.

Branching coral morphology affects physiological performance in the absence of colony integration.

For nearly 50 years, analyses of coral physiology have used small coral fragments (nubbins) to make inferences about larger colonies. However, scaling in corals shows that linear extrapolations from nubbins to whole colonies can be misleading, because polyps in nubbins are divorced of their morphologically complex and physiologically integrated corallum. We tested for the effects of integration among branches in determining size-dependent calcification of the coral Pocillopora spp. under elevated PCO2. Area-normalized net calcification was compared between branches (nubbins), aggregates of nubbins (complex morphologies without integration) and whole colonies (physiologically integrated) at 400 versus approximately 1000 µatm PCO2. Net calcification was unaffected by PCO2, but differed among colony types. Single nubbins grew faster than whole colonies, but when aggregated, nubbins changed calcification to match whole colonies even though they lacked integration among branches. Corallum morphology causes the phenotype of branching corals to differ from the summation of their branches.

Cophylogeny and specificity between cryptic coral species (Pocillopora spp.) at Mo'orea and their symbionts (Symbiodiniaceae).

The congruence between phylogenies of tightly associated groups of organisms (cophylogeny) reflects evolutionary links between ecologically important interactions. However, despite being a classic example of an obligate symbiosis, tests of cophylogeny between scleractinian corals and their photosynthetic algal symbionts have been hampered in the past because both corals and algae contain genetically unresolved and morphologically cryptic species. Here, we studied co-occurring, cryptic Pocillopora species from Mo'orea, French Polynesia, that differ in their relative abundance across depth. We constructed new phylogenies of the host Pocillopora (using complete mitochondrial genomes, genomic loci, and thousands of single nucleotide polymorphisms) and their Symbiodiniaceae symbionts (using ITS2 and psbAncr markers) and tested for cophylogeny. The analysis supported the presence of five Pocillopora species on the fore reef at Mo'orea that mostly hosted either Cladocopium latusorum or C. pacificum. Only Pocillopora species hosting C. latusorum also hosted taxa from Symbiodinium and Durusdinium. In general, the Cladocopium phylogeny mirrored the Pocillopora phylogeny. Within Cladocopium species, lineages also differed in their associations with Pocillopora haplotypes, except those showing evidence of nuclear introgression, and with depth in the two most common Pocillopora species. We also found evidence for a new Pocillopora species (haplotype 10), that has so far only been sampled from French Polynesia, that warrants formal identification. The linked phylogenies of these Pocillopora and Cladocopium species and lineages suggest that symbiont speciation is driven by niche diversification in the host, but there is still evidence for symbiont flexibility in some cases.

Behavioral Variability of Hatchlings Modifies Dispersal Potential in Crown Conch (Melongena corona): Why Do Larvae Crawl Away but Sometimes Swim?

AbstractThe diversity and consequences of development in marine invertebrates have, for a long time, provided the opportunity to understand different evolutionary solutions to living in variable environments. However, discrete classifications of development can impede a full understanding of adaptation to variable environments when behavioral, morphological, or physiological flexibility and variation exist within traditionally defined modes of development. We report here novel behavioral variability in hatchlings of a marine gastropod, the Florida crown conch (Melongena corona), that has broad significance for understanding the correlated evolution of development, dispersal, and reproductive strategies in variable environments. All hatchlings crawl away from egg capsules after emergence as larval pediveligers. Some subsequently swim for a brief period (seconds to minutes) before crawling again. From detailed observations of 120 individuals over 30 days, we observed 28 (23.3%) hatchlings swimming at least once (8%-50% per maternal brood). The propensity to swim was unrelated to time spent encapsulated or size at hatching and lasted for 22 days. We manipulated hypothesized environmental cues and found that the proportion of hatchlings that swam was highest in the absence of cues related to habitat or juvenile food and lowest when only habitat cues were present. The relative growth rate of hatchlings was highest when habitats contained a putative juvenile food source. About 44% of hatchlings were competent to metamorphose at emergence but did not metamorphose at this time in the lab or the field. The rate of metamorphosis increased with age and depended on the presence of unknown cues in the field. Crawl-away larvae with prolonged swimming ability may be an adaptation to balance the unpredictable risks of exclusively benthic or pelagic development and to allow the option to disperse to higher-quality habitat.

Response diversity in corals: hidden differences in bleaching mortality among cryptic Pocillopora species.

Variation among functionally similar species in their response to environmental stress buffers ecosystems from changing states. Functionally similar species may often be cryptic species representing evolutionarily distinct genetic lineages that are morphologically indistinguishable. However, the extent to which cryptic species differ in their response to stress, and could therefore provide a source of response diversity, remains unclear because they are often not identified or are assumed to be ecologically equivalent. Here, we uncover differences in the bleaching response between sympatric cryptic species of the common Indo-Pacific coral, Pocillopora. In April 2019, prolonged ocean heating occurred at Moorea, French Polynesia. 72% of pocilloporid colonies bleached after 22 d of severe heating (>8o C-days) at 10 m depth on the north shore fore reef. Colony mortality ranged from 11% to 42% around the island four months after heating subsided. The majority (86%) of pocilloporids that died from bleaching belonged to a single haplotype, despite twelve haplotypes, representing at least five species, being sampled. Mitochondrial (open reading frame) sequence variation was greater between the haplotypes that experienced mortality versus haplotypes that all survived than it was between nominal species that all survived. Colonies > 30 cm in diameter were identified as the haplotype experiencing the most mortality, and in 1125 colonies that were not genetically identified, bleaching and mortality increased with colony size. Mortality did not increase with colony size within the haplotype suffering the highest mortality, suggesting that size-dependent bleaching and mortality at the genus level was caused instead by differences among cryptic species. The relative abundance of haplotypes shifted between February and August, driven by declines in the same common haplotype for which mortality was estimated directly, at sites where heat accumulation was greatest, and where larger colony sizes occurred. The identification of morphologically indistinguishable species that differ in their response to thermal stress, but share a similar ecological function in terms of maintaining a coral-dominated state, has important consequences for uncovering response diversity that drives resilience, especially in systems with low or declining functional diversity.

Global biogeography of marine dispersal potential.

The distance travelled by marine larvae varies by seven orders of magnitude. Dispersal shapes marine biodiversity, and must be understood if marine systems are to be well managed. Because warmer temperatures quicken larval development, larval durations might be systematically shorter in the tropics relative to those at high latitudes. Nevertheless, life history and hydrodynamics also covary with latitude-these also affect dispersal, precluding any clear expectation of how dispersal changes at a global scale. Here we combine data from the literature encompassing >750 marine organisms from seven phyla with oceanographic data on current speeds, to quantify the overall latitudinal gradient in larval dispersal distance. We find that planktonic duration increased with latitude, confirming predictions that temperature effects outweigh all others across global scales. However, while tropical species have the shortest planktonic durations, realized dispersal distances were predicted to be greatest in the tropics and at high latitudes, and lowest at mid-latitudes. At high latitudes, greater dispersal distances were driven by moderate current speed and longer planktonic durations. In the tropics, fast currents overwhelmed the effect of short planktonic durations. Our results contradict previous hypotheses based on biology or physics alone; rather, biology and physics together shape marine dispersal patterns.

Inbreeding shapes the evolution of marine invertebrates.

Inbreeding is a potent evolutionary force shaping the distribution of genetic variation within and among populations of plants and animals. Yet, our understanding of the forces shaping the expression and evolution of nonrandom mating in general, and inbreeding in particular, remains remarkably incomplete. Most research on plant mating systems focuses on self-fertilization and its consequences for automatic selection, inbreeding depression, purging, and reproductive assurance, whereas studies of animal mating systems have often assumed that inbreeding is rare, and that natural selection favors traits that promote outbreeding. Given that many sessile and sedentary marine invertebrates and marine macroalgae share key life history features with seed plants (e.g., low mobility, modular construction, and the release of gametes into the environment), their mating systems may be similar. Here, we show that published estimates of inbreeding coefficients (FIS ) for sessile and sedentary marine organisms are similar and at least as high as noted in terrestrial seed plants. We also found that variation in FIS within invertebrates is related to the potential to self-fertilize, disperse, and choose mates. The similarity of FIS for these organismal groups suggests that inbreeding could play a larger role in the evolution of sessile and sedentary marine organisms than is currently recognized. Specifically, associations between traits of marine invertebrates and FIS suggest that inbreeding could drive evolutionary transitions between hermaphroditism and separate sexes, direct development and multiphasic life cycles, and external and internal fertilization.

Emergent properties of branching morphologies modulate the sensitivity of coral calcification to high PCO2.

Experiments with coral fragments (i.e. nubbins) have shown that net calcification is depressed by elevated PCO2 Evaluating the implications of this finding requires scaling of results from nubbins to colonies, yet the experiments to codify this process have not been carried out. Building from our previous research demonstrating that net calcification of Pocillopora verrucosa (2-13 cm diameter) was unaffected by PCO2  (400 and 1000 µatm) and temperature (26.5 and 29.7°C), we sought generality to this outcome by testing how colony size modulates PCO2  and temperature sensitivity in a branching acroporid. Together, these taxa represent two of the dominant lineages of branching corals on Indo-Pacific coral reefs. Two trials conducted over 2 years tested the hypothesis that the seasonal range in seawater temperature (26.5 and 29.2°C) and a future PCO2  (1062 µatm versus an ambient level of 461 µatm) affect net calcification of an ecologically relevant size range (5-20 cm diameter) of colonies of Acropora hyacinthus As for P. verrucosa, the effects of temperature and PCO2  on net calcification (mg day-1) of A. verrucosa were not statistically detectable. These results support the generality of a null outcome on net calcification of exposing intact colonies of branching corals to environmental conditions contrasting seasonal variation in temperature and predicted future variation in PCO2 While there is a need to expand beyond an experimental culture relying on coral nubbins as tractable replicates, rigorously responding to this need poses substantial ethical and logistical challenges.

How relatedness between mates influences reproductive success: An experimental analysis of self-fertilization and biparental inbreeding in a marine bryozoan.

Kin associations increase the potential for inbreeding. The potential for inbreeding does not, however, make inbreeding inevitable. Numerous factors influence whether inbreeding preference, avoidance, or tolerance evolves, and, in hermaphrodites where both self-fertilization and biparental inbreeding are possible, it remains particularly difficult to predict how selection acts on the overall inbreeding strategy, and to distinguish the type of inbreeding when making inferences from genetic markers. Therefore, we undertook an empirical analysis on an understudied type of mating system (spermcast mating in the marine bryozoan, Bugula neritina) that provides numerous opportunities for inbreeding preference, avoidance, and tolerance. We created experimental crosses, containing three generations from two populations to estimate how parental reproductive success varies across parental relatedness, ranging from self, siblings, and nonsiblings from within the same population. We found that the production of viable selfed offspring was extremely rare (only one colony produced three selfed offspring) and biparental inbreeding more common. Paternity analysis using 16 microsatellite markers confirmed outcrossing. The production of juveniles was lower for sib mating compared with nonsib mating. We found little evidence for consistent inbreeding, in terms of nonrandom mating, in adult samples collected from three populations, using multiple population genetic inferences. Our results suggest several testable hypotheses that potentially explain the overall mating and dispersal strategy in this species, including early inbreeding depression, inbreeding avoidance through cryptic mate choice, and differential dispersal distances of sperm and larvae.

Size-dependent physiological responses of the branching coral Pocillopora verrucosa to elevated temperature and PCO2.

Body size has large effects on organism physiology, but these effects remain poorly understood in modular animals with complex morphologies. Using two trials of a ∼24 day experiment conducted in 2014 and 2015, we tested the hypothesis that colony size of the coral Pocillopora verrucosa affects the response of calcification, aerobic respiration and gross photosynthesis to temperature (∼26.5 and ∼29.7°C) and PCO2  (∼40 and ∼1000 µatm). Large corals calcified more than small corals, but at a slower size-specific rate; area-normalized calcification declined with size. Whole-colony and area-normalized calcification were unaffected by temperature, PCO2 , or the interaction between the two. Whole-colony respiration increased with colony size, but the slopes of these relationships differed between treatments. Area-normalized gross photosynthesis declined with colony size, but whole-colony photosynthesis was unaffected by PCO2 , and showed a weak response to temperature. When scaled up to predict the response of large corals, area-normalized metrics of physiological performance measured using small corals provide inaccurate estimates of the physiological performance of large colonies. Together, these results demonstrate the importance of colony size in modulating the response of branching corals to elevated temperature and high PCO2.

Global change, life-history complexity and the potential for evolutionary rescue.

Most organisms have complex life cycles, and in marine taxa, larval life-history stages tend to be more sensitive to environmental stress than adult (reproductive) life-history stages. While there are several models of stage-specific adaptation across the life history, the extent to which differential sensitivity to environmental stress (defined here as reductions in absolute fitness across the life history) affects the tempo of adaptive evolution to change remains unclear. We used a heuristic model to explore how commonly observed features associated with marine complex life histories alter a population's capacity to cope with environmental change. We found that increasing the complexity of the life history generally reduces the evolutionary potential of taxa to cope with environmental change. Our model also predicted that genetic correlations in stress tolerance between stages, levels of genetic variance in each stage, and the relative plasticity of different stages, all interact to affect the maximum rate of environmental change that will permit species persistence. Our results suggest that marine organisms with complex life cycles are particularly vulnerable to anthropogenic global change, but we lack empirical estimates of key parameters for most species.

When is dispersal for dispersal? Unifying marine and terrestrial perspectives.

Recent syntheses on the evolutionary causes of dispersal have focused on dispersal as a direct adaptation, but many traits that influence dispersal have other functions, raising the question: when is dispersal 'for' dispersal? We review and critically evaluate the ecological causes of selection on traits that give rise to dispersal in marine and terrestrial organisms. In the sea, passive dispersal is relatively easy and specific morphological, behavioural, and physiological adaptations for dispersal are rare. Instead, there may often be selection to limit dispersal. On land, dispersal is relatively difficult without specific adaptations, which are relatively common. Although selection for dispersal is expected in both systems and traits leading to dispersal are often linked to fitness, systems may differ in the extent to which dispersal in nature arises from direct selection for dispersal or as a by-product of selection on traits with other functions. Our analysis highlights incompleteness of theories that assume a simple and direct relationship between dispersal and fitness, not just insofar as they ignore a vast array of taxa in the marine realm, but also because they may be missing critically important effects of traits influencing dispersal in all realms.

Deconstructing environmental predictability: seasonality, environmental colour and the biogeography of marine life histories.

Environmental predictability is predicted to shape the evolution of life histories. Two key types of environmental predictability, seasonality and environmental colour, may influence life-history evolution independently but formal considerations of both and how they relate to life history are exceedingly rare. Here, in a global biogeographical analysis of over 800 marine invertebrates, we explore the relationships between both forms of environmental predictability and three fundamental life-history traits: location of larval development (aplanktonic vs. planktonic), larval developmental mode (feeding vs. non-feeding) and offspring size. We found that both dispersal potential and offspring size related to environmental predictability, but the relationships depended on both the environmental factor as well as the type of predictability. Environments that were more seasonal in food availability had a higher prevalence of species with a planktonic larval stage. Future studies should consider both types of environmental predictability as each can strongly affect life-history evolution.

Beyond connectivity: how empirical methods can quantify population persistence to improve marine protected-area design.

Demographic connectivity is a fundamental process influencing the dynamics and persistence of spatially structured populations. Consequently, quantifying connectivity is essential for properly designing networks of protected areas so that they achieve their core ecological objective of maintaining population persistence. Recently, many empirical studies in marine systems have provided essential, and historically challenging to obtain, data on patterns of larval dispersal and export from marine protected areas (MPAs). Here, we review the empirical studies that have directly quantified the origins and destinations of individual larvae and assess those studies' relevance to the theory of population persistence and MPA design objectives. We found that empirical studies often do not measure or present quantities that are relevant to assessing population persistence, even though most studies were motivated or contextualized by MPA applications. Persistence of spatial populations, like nonspatial populations, depends on replacement, whether individuals reproduce enough in their lifetime to replace themselves. In spatial populations, one needs to account for the effect of larval dispersal on future recruitment back to the local population through local retention and other connectivity pathways. The most commonly reported descriptor of larval dispersal was the fraction of recruitment from local origin (self-recruitment). Self-recruitment does not inform persistence-based MPA design because it is a fraction of those arriving, not a fraction of those leaving (local retention), so contains no information on replacement. Some studies presented connectivity matrices, which can inform assessments of persistence with additional knowledge of survival and fecundity after recruitment. Some studies collected data in addition to larval dispersal that could inform assessments of population persistence but which were not presented in that way. We describe how three pieces of empirical information are needed to fully describe population persistence in a network of MPAs: (1) lifetime fecundity, (2) the proportion of larvae that are locally retained (or the full connectivity matrix), and (3) survival rate after recruitment. We conclude by linking theory and data to provide detailed guidance to empiricists and practitioners on field sampling design and data presentation that better informs the MPA objective of population persistence.

Assessing strategies to minimize unintended fitness consequences of aquaculture on wild populations.

Artificial propagation programs focused on production, such as commercial aquaculture or forestry, entail strong domestication selection. Spillover from such programs can cause unintended fitness and demographic consequences for wild conspecifics. The range of possible management practices to minimize such consequences vary in their control of genetic and demographic processes. Here, we use a model of coupled genetic and demographic dynamics to evaluate alternative management approaches to minimizing unintended consequences of aquaculture escapees. We find that, if strong natural selection occurs between escape and reproduction, an extremely maladapted (i.e., nonlocal-origin, highly domesticated) stock could have fitness consequences analogous to a weakly diverged cultured stock; otherwise, wild population fitness declines with increasing maladaptation in the cultured stock. Reducing escapees through low-level leakage is more effective than reducing an analogous number of escapees from large, rare pulses. This result arises because low-level leakage leads to the continual lowering of wild population fitness and subsequent increased proportional contribution of maladapted cultured escapees to the total population. Increased sterilization efficacy can cause rapid, nonlinear reductions in unintended fitness consequences. Finally, sensitivity to the stage of escape indicates a need for improved monitoring data on how the number of escapees varies across life cycle stages.