Rampant asexual reproduction and limited dispersal in a mangrove population of the coral Porites divaricata.

Corals are critical to marine biodiversity. Reproduction and dispersal are key to their resilience, but rarely quantified in nature. Exploiting a unique system-a fully censused, longitudinally characterized, semi-isolated population inhabiting mangroves-we used 2bRAD sequencing to demonstrate that rampant asexual reproduction most likely via parthenogenesis and limited dispersal enable the persistence of a natural population of thin-finger coral (Porites divaricata). Unlike previous studies on coral dispersal, knowledge of colony age and location enabled us to identify plausible parent-offspring relationships within multiple clonal lineages and develop tightly constrained estimates of larval dispersal; the best-fitting model indicates dispersal is largely limited to a few metres from parent colonies. Our results explain why this species is adept at colonizing mangroves but suggest limited genetic diversity in mangrove populations and limited connectivity between mangroves and nearby reefs. As P. divaricata is gonochoristic, and parthenogenesis would be restricted to females (whereas fragmentation, which is presumably common in reef and seagrass habitats, is not), mangrove populations likely exhibit skewed sex ratios. These findings suggest that coral reproductive diversity can lead to distinctly different demographic outcomes in different habitats. Thus, coral conservation will require the protection of the entire coral habitat mosaic, and not just reefs.

Review of housing and husbandry of anemonefishes for use in research.

Anemonefishes of the genus Amphiprion are emerging as a model organism for marine science, so there is potentially a lot for the research community to gain by optimizing and standardizing housing and husbandry protocols. Here, we conducted a literature review and a questionnaire survey regarding the housing and husbandry of anemonefishes for use in research. The questionnaire survey was completed by 27 laboratories, with a 45% response rate, across 11 different countries in Europe, North America, Asia and Australia. Results from the literature review identified that housing and husbandry protocols varied widely in terms of tank volume, diet composition and lighting type for the housing of broodstock pairs. These results also emphasize the significant impacts that variation in housing and husbandry protocols have on fish. Results from the questionnaire survey confirmed this. We identified multiple opportunities for improvement of protocols, including the potential for exchange of larvae between laboratories to create strains and reduce pressure on natural populations. In conclusion, our research suggests that the anemonefish research community should be discussing the optimization and standardization of housing and husbandry or, minimally, recognizing that housing and husbandry influence a wide range of traits and will influence the results and conclusions drawn from experiments.

Heritability of dispersal-related larval traits in the clown anemonefish Amphiprion percula.

A major goal of marine ecology is to identify the drivers of variation in larval dispersal. Larval traits are emerging as an important potential source of variation in dispersal outcomes, but little is known about how the evolution of these traits might shape dispersal patterns. Here, we consider the potential for adaptive evolution in two possibly dispersal-related traits by quantifying the heritability of larval size and swimming speed in the clown anemonefish (Amphiprion percula). Using a laboratory population of wild-caught A. percula, we measured the size and swimming speed of larvae from 24 half-sibling families. Phenotypic variance was partitioned into genetic and environmental components using a linear mixed-effects model. Importantly, by including half-siblings in the breeding design, we ensured that our estimates of genetic variance do not include nonheritable effects shared by clutches of full-siblings, which could lead to significant overestimates of heritability. We find unequivocal evidence for the heritability of larval body size (estimated between 0.21 and 0.34) and equivocal evidence for the heritability of swimming speed (between 0.05 and 0.19 depending on the choice of prior). From a methodological perspective, this work demonstrates the importance of evaluating sensitivity to prior distribution in Bayesian analysis. From a biological perspective, it advances our understanding of potential dispersal-related larval traits by quantifying the extent to which they can be inherited and thus have the potential for adaptive evolution.

Paternal care regulates the timing, synchrony and success of hatching in a coral reef fish.

In oviparous species, the timing of hatching is a crucial decision, but for developing embryos, assessing cues that indicate the optimal time to hatch is challenging. In species with pre-hatching parental care, parents can assess environmental conditions and induce their offspring to hatch. We provide the first documentation of parental hatching regulation in a coral reef fish, demonstrating that male neon gobies (Elacatinus colini) directly regulate hatching by removing embryos from the clutch and spitting hatchlings into the water column. All male gobies synchronized hatching within 2 h of sunrise, regardless of when eggs were laid. Paternally incubated embryos hatched later in development, more synchronously, and had higher hatching success than artificially incubated embryos that were shaken to provide a vibrational stimulus or not stimulated. Artificially incubated embryos displayed substantial plasticity in hatching times (range: 80-224 h post-fertilization), suggesting that males could respond to environmental heterogeneity by modifying the hatching time of their offspring. Finally, paternally incubated embryos hatched with smaller yolk sacs and larger propulsive areas than artificially incubated embryos, suggesting that paternal effects on hatchling phenotypes may influence larval dispersal and fitness. These findings highlight the complexity of fish parental care behaviour and may have important, and currently unstudied, consequences for fish population dynamics.

Vertebrate growth plasticity in response to variation in a mutualistic interaction.

Vertebrate growth can be phenotypically plastic in response to predator-prey and competitive interactions. It is unknown however, if it can be plastic in response to mutualistic interactions. Here we investigate plasticity of vertebrate growth in response to variation in mutualistic interactions, using clown anemonefish and their anemone hosts. In the wild, there is a positive correlation between the size of the fish and the size of the anemone, but the cause of this correlation is unknown. Plausible hypotheses are that fish exhibit growth plasticity in response to variation in food or space provided by the host. In the lab, we pair individuals with real anemones of various sizes and show that fish on larger anemones grow faster than fish on smaller anemones. By feeding the fish a constant food ration, we exclude variation in food availability as a cause. By pairing juveniles with artificial anemones of various sizes, we exclude variation in space availability as a single cause. We argue that variation in space availability in conjunction with host cues cause the variability in fish growth. By adjusting their growth, anemonefish likely maximize their reproductive value given their anemone context. More generally, we demonstrate vertebrate growth plasticity in response to variation in mutualistic interactions.

Strategic growth in social vertebrates.

Individual differences in growth and size of vertebrates often represent adaptive, plastic responses to contrasts in ecological conditions. Recent studies show that vertebrates can also modify their growth and size in an adaptive fashion in response to fine-grain changes in social conditions (which we refer to as strategic growth). Here, we review experimental evidence for strategic growth in social vertebrates. We describe a set of conditions under which strategic growth commonly occurs, and highlight potential examples of convergent evolution of strategic growth across the tree of life. This synthesis has implications for the way we think about organismal growth and size, because it underscores that the size of individuals can often be fine-tuned to their social environment.

An integrative investigation of sensory organ development and orientation behavior throughout the larval phase of a coral reef fish.

The dispersal of marine larvae determines the level of connectivity among populations, influences population dynamics, and affects evolutionary processes. Patterns of dispersal are influenced by both ocean currents and larval behavior, yet the role of behavior remains poorly understood. Here we report the first integrated study of the ontogeny of multiple sensory systems and orientation behavior throughout the larval phase of a coral reef fish-the neon goby, Elacatinus lori. We document the developmental morphology of all major sensory organs (lateral line, visual, auditory, olfactory, gustatory) together with the development of larval swimming and orientation behaviors observed in a circular arena set adrift at sea. We show that all sensory organs are present at hatch and increase in size (or number) and complexity throughout the larval phase. Further, we demonstrate that most larvae can orient as early as 2 days post-hatch, and they swim faster and straighter as they develop. We conclude that sensory organs and swimming abilities are sufficiently developed to allow E. lori larvae to orient soon after hatch, suggesting that early orientation behavior may be common among coral reef fishes. Finally, we provide a framework for testing alternative hypotheses for the orientation strategies used by fish larvae, laying a foundation for a deeper understanding of the role of behavior in shaping dispersal patterns in the sea.

Genetic relatedness in social groups of the emerald coral goby Paragobiodon xanthosoma creates potential for weak kin selection.

Animals forming social groups that include breeders and nonbreeders present evolutionary paradoxes; why do breeders tolerate nonbreeders? And why do nonbreeders tolerate their situation? Both paradoxes are often explained with kin selection. Kin selection is, however, assumed to play little or no role in social group formation of marine organisms with dispersive larval phases. Yet, in some marine organisms, recent evidence suggests small-scale patterns of relatedness, meaning that this assumption must always be tested. Here, we investigated the genetic relatedness of social groups of the emerald coral goby, Paragobiodon xanthosoma. We genotyped 73 individuals from 16 groups in Kimbe Bay, Papua New Guinea, at 20 microsatellite loci and estimated pairwise relatedness among all individuals. We found that estimated pairwise relatedness among individuals within groups was significantly higher than the pairwise relatedness among individuals from the same reef, and pairwise relatedness among individuals from the same reef was significantly higher than the pairwise relatedness among individuals from different reefs. This spatial signature suggests that there may be very limited dispersal in this species. The slightly positive relatedness within groups creates the potential for weak kin selection, which may help to resolve the paradox of why breeders tolerate subordinates in P. xanthosoma. The other paradox, why nonbreeders tolerate their situation, is better explained by alternative hypotheses such as territory inheritance, and ecological and social constraints. We show that even in marine animals with dispersive larval phases, kin selection needs to be considered to explain the evolution of complex social groups.

Ecological and social constraints combine to promote evolution of non-breeding strategies in clownfish.

Individuals that forgo their own reproduction in animal societies represent an evolutionary paradox because it is not immediately apparent how natural selection can preserve the genes that underlie non-breeding strategies. Cooperative breeding theory provides a solution to the paradox: non-breeders benefit by helping relatives and/or inheriting breeding positions; non-breeders do not disperse to breed elsewhere because of ecological constraints. However, the question of why non-breeders do not contest to breed within their group has rarely been addressed. Here, we use a wild population of clownfish (Amphiprion percula), where non-breeders wait peacefully for years to inherit breeding positions, to show non-breeders will disperse when ecological constraints (risk of mortality during dispersal) are experimentally weakened. In addition, we show non-breeders will contest when social constraints (risk of eviction during contest) are experimentally relaxed. Our results show it is the combination of ecological and social constraints that promote the evolution of non-breeding strategies. The findings highlight parallels between, and potential for fruitful exchange between, cooperative breeding theory and economic bargaining theory: individuals will forgo their own reproduction and wait peacefully to inherit breeding positions (engage in cooperative options) when there are harsh ecological constraints (poor outside options) and harsh social constraints (poor inside options).

Sensory cues underlying competitive growth in the clown anemonefish (Amphiprion percula).

In some animal societies, access to breeding depends on the individual's position in a hierarchy, which often depends on an individual's size. In such societies, individuals may try to outgrow one another to attain a higher rank by engaging in a form of strategic growth (competitive growth). This suggests that members of the hierarchy can track changes in the growth and size of potential competitors and respond accordingly. The clown anemonefish, Amphiprion percula, is one species known to exhibit competitive growth at the initiation of size hierarchies. Here, we use 5 combinations of sensory cues to determine which cues must be available for individuals to engage in competitive growth. Our results show that mechanosensory (pressure and/or touch) cues or unobstructed interactions are necessary for competitive growth to occur. This study provides an understanding of the relationship between sensory cues and phenotypic responses to different social contexts.

Natal philopatry increases relatedness within groups of coral reef cardinalfish.

A central issue in evolutionary ecology is how patterns of dispersal influence patterns of relatedness in populations. In terrestrial organisms, limited dispersal of offspring leads to groups of related individuals. By contrast, for most marine organisms, larval dispersal in open waters is thought to minimize kin associations within populations. However, recent molecular evidence and theoretical approaches have shown that limited dispersal, sibling cohesion and/or differential reproductive success can lead to kin association and elevated relatedness. Here, we tested the hypothesis that limited dispersal explains small-scale patterns of relatedness in the pajama cardinalfish Sphaeramia nematoptera. We used 19 microsatellite markers to assess parentage of 233 juveniles and pairwise relatedness among 527 individuals from 41 groups in Kimbe Bay, Papua New Guinea. Our findings support three predictions of the limited dispersal hypothesis: (i) elevated relatedness within groups, compared with among groups and elevated relatedness within reefs compared with among reefs; (ii) a weak negative correlation of relatedness with distance; (iii) more juveniles than would be expected by chance in the same group and the same reef as their parents. We provide the first example for natal philopatry at the group level causing small-scale patterns of genetic relatedness in a marine fish.

Unraveling hierarchical genetic structure in a marine metapopulation: A comparison of three high-throughput genotyping approaches.

Marine metapopulations often exhibit subtle population structure that can be difficult to detect. Given recent advances in high-throughput sequencing, an emerging question is whether various genotyping approaches, in concert with improved sampling designs, will substantially improve our understanding of genetic structure in the sea. To address this question, we explored hierarchical patterns of structure in the coral reef fish Elacatinus lori using a high-resolution approach with respect to both genetic and geographic sampling. Previously, we identified three putative E. lori populations within Belize using traditional genetic markers and sparse geographic sampling: barrier reef and Turneffe Atoll; Glover's Atoll; and Lighthouse Atoll. Here, we systematically sampled individuals at ~10 km intervals throughout these reefs (1,129 individuals from 35 sites) and sequenced all individuals at three sets of markers: 2,418 SNPs; 89 microsatellites; and 57 nonrepetitive nuclear loci. At broad spatial scales, the markers were consistent with each other and with previous findings. At finer spatial scales, there was new evidence of genetic substructure, but our three marker sets differed slightly in their ability to detect these patterns. Specifically, we found subtle structure between the barrier reef and Turneffe Atoll, with SNPs resolving this pattern most effectively. We also documented isolation by distance within the barrier reef. Sensitivity analyses revealed that the number of loci (and alleles) had a strong effect on the detection of structure for all three marker sets, particularly at small spatial scales. Taken together, these results illustrate empirically that high-throughput genotyping data can elucidate subtle genetic structure at previously-undetected scales in a dispersive marine fish.

Hydrodynamic and biological constraints on group cohesion in plankton.

The dynamics of plankton in the ocean are determined by biophysical interactions. Although physics and biotic behaviors are known to influence the observed patchiness of planktonic populations, it is still unclear how much, and if, group behavior contributes to this biophysical interaction. Here, we demonstrate how simple rules of behavior can enhance or inhibit active group cohesion in plankton in a turbulent environment. In this study, we used coral-reef fish larvae as a model to investigate the interaction between microscale turbulence and planktonic organisms. We synthesized available information on the swimming speeds and sizes of reef fish larvae, and developed a set of equations to investigate the effects of viscosity and turbulence on larvae dispersion. We then calculated the critical dispersion rates for three different swimming strategies - cruise, random-walk, and pause-travel - to determine which strategies could facilitate group cohesion during dispersal. Our results indicate that swimming strategies and migration to low-turbulence regions are the key to maintaining group cohesion, suggesting that many reef fish species have the potential to remain together, from hatching to settlement. In addition, larvae might change their swimming strategies to maintain group cohesion, depending on environmental conditions and/or their ontogenic stage. This study provides a better understanding of the hydrodynamic and biological constraints on group formation and cohesion in planktonic organisms, and reveals a wide range of conditions under which group formation may occur.

Competitive growth in a social fish.

Many animal societies have dominance hierarchies in which social rank is correlated with size. In such societies, the growth and size of individuals can be a strategic response to their social environment: in fishes, individuals may decrease their growth rate to remain small and retain a subordinate position; in mammals, individuals may increase their growth rate to become large and attain a dominant position-a strategy called competitive growth. Here, we investigate whether the clown anemonefish, Amphiprion percula, exhibits competitive growth also. We show that juvenile clownfish paired with a size-matched reproductive rival increase their growth rate and size relative to solitary controls. Remarkably, paired individuals achieved this, despite being provided with the same amount of food as solitary controls. Our results demonstrate that clownfish are able to increase their growth rate in response to social competition. This study adds to the growing body of evidence that the growth of social vertebrates can be a fine-tuned plastic response to their social environment.

Comparison of efficiency of direct observations by scuba diver and indirect observations via video camera for measuring reef-fish behaviour.

The present study investigates how the humbug damselfish Dascyllus aruanus, subject of a large number of ecological, evolutionary and behavioural studies, responds to the presence of human observers (effect of scuba diver presence-absence) and how the method of data collection (directly by a scuba diver v. indirectly via video camera) may affect the quality of behavioural data. Scuba diver presence had only subtle effects on fish behaviour. The efficiency of the method of scoring fish behaviour depended on the behaviour under consideration: those behaviours that occur in close proximity to the corals were scored more effectively directly by a scuba diver while those that are performed in a more rapid or repetitive fashion were scored more effectively indirectly via video camera. These results provide a foundation for future behavioural research on D. aruanus and other fishes where scuba divers or video cameras are the prevalent means of data collection.

The Evolution of Marine Larval Dispersal Kernels in Spatially Structured Habitats: Analytical Models, Individual-Based Simulations, and Comparisons with Empirical Estimates.

Understanding the causes of larval dispersal is a major goal of marine ecology, yet most research focuses on proximate causes. Here we ask how ultimate, evolutionary causes affect dispersal. Building on Hamilton and May's classic 1977 article "Dispersal in Stable Habitats," we develop analytic and simulation models for the evolution of dispersal kernels in spatially structured habitats. First, we investigate dispersal in a world without edges and find that most offspring disperse as far as possible, opposite the pattern of empirical data. Adding edges to our model world leads to nearly all offspring dispersing short distances, again a mismatch with empirical data. Adding resource heterogeneity improves our results: most offspring disperse short distances with some dispersing longer distances. Finally, we simulate dispersal evolution in a real seascape in Belize and find that the simulated dispersal kernel and an empirical dispersal kernel from that seascape both have the same shape, with a high level of short-distance dispersal and a low level of long-distance dispersal. The novel contributions of this work are to provide a spatially explicit analytic extension of Hamilton and May's 1977 work, to demonstrate that our spatially explicit simulations and analytic models provide equivalent results, and to use simulation approaches to investigate the evolution of dispersal kernel shape in spatially complex habitats. Our model could be modified in various ways to investigate dispersal evolution in other species and seascapes, providing new insights into patterns of marine larval dispersal.

Potential roles of smell and taste in the orientation behaviour of coral-reef fish larvae: insights from morphology.

An ontogenetic analysis of the olfactory organ and the number and distribution of internal taste buds was carried out in two neon gobies (Elacatinus lori and Elacatinus colini) with the goal of revealing morphological trends that might inform an understanding of the roles of olfaction and taste in larval orientation behaviour. The pattern of development of the olfactory organ is unremarkable and enclosure of the olfactory epithelium occurs concurrently with metamorphosis and settlement in both species. Like other gobies, juvenile and adult E. lori and E. colini lack complex olfactory lamellae, and lack the accessory nasal sacs present in some adult gobies that could facilitate active olfactory ventilation (i.e., sniffing). A small number of internal taste buds are present at hatch with most found in the caudal region of the buccal cavity (on gill arches, roof of buccal cavity). As taste bud number increases, they demonstrate an anterior spread to the lips, buccal valves and tongue (i.e., tissue covering the basihyal). In the absence of an active ventilatory mechanism for the olfactory organs, the water that moves through the buccal cavity with cyclic gill ventilation may provide chemical cues allowing the internal taste buds to play a role in chemical-mediated orientation and reef-seeking behavior in pelagic larval fishes.

Offspring sex preferences among patrilineal and matrilineal Mosuo in Southwest China revealed by differences in parity progression.

Son preference predominates in China, yet there are patterned exceptions to this rule. In this paper, we test whether lineality (patrilineal versus matrilineal inheritance and descent) is associated with son versus daughter preference among the ethnic Mosuo (Na) of Southwest China. Our results show (i) an increased probability of continued fertility among matrilineal women after having a son compared with a daughter and (ii) an increased probability of continued fertility among patrilineal women after having a daughter compared with a son. These results are consistent with son preference among patrilineal Mosuo and more muted daughter preference among the matrilineal Mosuo. Furthermore, we show (iii) the lowest probability of continued fertility at parity 2 once women have one daughter and one son across both systems, suggesting that preferences for at least one of each sex exist alongside preferences for the lineal sex. The Mosuo are the only known small-scale society in which two kinship systems distinguish sub-groups with many otherwise shared cultural characteristics. We discuss why this, in conjunction with differences in subsistence, may shed light on the evolutionary underpinnings of offspring sex preferences.

Patterns, causes, and consequences of marine larval dispersal.

Quantifying the probability of larval exchange among marine populations is key to predicting local population dynamics and optimizing networks of marine protected areas. The pattern of connectivity among populations can be described by the measurement of a dispersal kernel. However, a statistically robust, empirical dispersal kernel has been lacking for any marine species. Here, we use genetic parentage analysis to quantify a dispersal kernel for the reef fish Elacatinus lori, demonstrating that dispersal declines exponentially with distance. The spatial scale of dispersal is an order of magnitude less than previous estimates-the median dispersal distance is just 1.7 km and no dispersal events exceed 16.4 km despite intensive sampling out to 30 km from source. Overlaid on this strong pattern is subtle spatial variation, but neither pelagic larval duration nor direction is associated with the probability of successful dispersal. Given the strong relationship between distance and dispersal, we show that distance-driven logistic models have strong power to predict dispersal probabilities. Moreover, connectivity matrices generated from these models are congruent with empirical estimates of spatial genetic structure, suggesting that the pattern of dispersal we uncovered reflects long-term patterns of gene flow. These results challenge assumptions regarding the spatial scale and presumed predictors of marine population connectivity. We conclude that if marine reserve networks aim to connect whole communities of fishes and conserve biodiversity broadly, then reserves that are close in space (<10 km) will accommodate those members of the community that are short-distance dispersers.

Marine ecology: reaping the benefits of local dispersal.

A central question of marine ecology is, how far do larvae disperse? Evidence is accumulating that the probability of dispersal declines rapidly with distance. This provides an incentive for communities to manage their own fish stocks and cooperate with neighbors.