Transcriptome‐based target‐enrichment baits for stony corals (Cnidaria: Anthozoa: Scleractinia)

Despite the ecological and economic significance of stony corals (Scleractinia), a robust understanding of their phylogeny remains elusive due to patchy taxonomic and genetic sampling, as well as the limited availability of informative markers. To increase the number of genetic loci available for phylogenomic analyses in Scleractinia, we designed 15,919 DNA enrichment baits targeting 605 orthogroups (mean 565 ± SD 366 bp) over 1,139 exon regions. A further 236 and 62 barcoding baits were designed for COI and histone H3 genes respectively for quality and contamination checks. Hybrid capture using these baits was performed on 18 coral species spanning the presently understood scleractinian phylogeny, with two corallimorpharians as outgroup. On average, 74% of all loci targeted were successfully captured for each species. Barcoding baits were matched unambiguously to their respective samples and revealed low levels of cross‐contamination in accordance with expectation. We put the data through a series of stringent filtering steps to ensure only scleractinian and phylogenetically informative loci were retained, and the final probe set comprised 13,479 baits, targeting 452 loci (mean 531 ± SD 307 bp) across 865 exon regions. Maximum likelihood, Bayesian and species tree analyses recovered maximally supported, topologically congruent trees consistent with previous phylogenomic reconstructions. The phylogenomic method presented here allows for consistent capture of orthologous loci among divergent coral taxa, facilitating the pooling of data from different studies and increasing the phylogenetic sampling of scleractinians in the future.     

Molecular and morphological supertree of stony corals (Anthozoa: Scleractinia) using matrix representation parsimony

The supertree algorithm matrix representation with parsimony was used to combine existing hypotheses of coral relationships and provide the most comprehensive species-level estimate of scleractinian phylogeny, comprised of 353 species (27% of extant species), 141 genera (63%) and 23 families (92%) from all seven suborders. The resulting supertree offers a guide for future studies in coral systematics by highlighting regions of concordance and conflict in existing source phylogenies. It should also prove useful in formal comparative studies of character evolution. Phylogenetic effort within Scleractinia has been taxonomically uneven, with a third of studies focussing on the Acroporidae or its most diverse genera. Sampling has also been geographically non-uniform, as tropical, reef-forming taxa have been considered twice as often as non-reef species. The supertree indicated that source trees concur on numerous aspects of coral relationships, such as the division between robust versus complex corals and the distant relationship between families in Archaeocoeniina. The supertree also supported the existence of a large, taxonomically diverse and monophyletic group of corals with many Atlantic representatives having exsert corallites. Another large, unanticipated clade consisted entirely of solitary deep-water species from three families. Important areas of ambiguity include the relationship of Astrocoeniidae to Pocilloporidae and the relative positions of several, mostly deep-water genera of Caryophylliidae. Conservative grafting of species at the base of congeneric groups with uncontroversial monophyletic status resulted in a more comprehensive, though less resolved tree of 1016 taxa.     

Sperm ultrastructure of a member of the black coral family Aphanipathidae: Rhipidipathes reticulata (Anthozoa, Antipatharia)

Fertile male polyps of three colonies of the black coral Rhipidipathes reticulata (Aphanipathidae) from Togian Islands (Indonesia) have been the source of the sperm investigated at ultrastructural level, in order to compare their organization with that of other members belonging to the family Antipathidae and Myriopathidae. The extension of the studies to a representative of the family Aphanipathidae stresses once more the structural similarity of the male gametes in antipatharians. A sketch of the sperm model reports the similarity and differences in the examined taxa. Among the micro-characters, the cup-like body linked to the pericentriolar apparatus, is exclusive of the antipatharians. Other inclusions concern the more common pro-acrosomal vesicles or the acrosomelike structure observed only in Antipathella subpinnata and Myriopathes japonica. Lipid vesicles are occasionally present. A typical inclusion, the electron-dense content of which has a C-shaped configuration, is restricted to Rhipidipathes reticulata and is associated to the cup-like body or to the mitochondrion.     

Slow mitochondrial DNA sequence evolution in the Anthozoa (Cnidaria)

Mitochondrial genes have been used extensively in population genetic and phylogeographical analyses, in part due to a high rate of nucleotide substitution in animal mitochondrial DNA (mtDNA). Nucleotide sequences of anthozoan mitochondrial genes, however, are virtually invariant among conspecifics, even at third codon positions of protein-coding sequences. Hence, mtDNA markers are of limited use for population-level studies in these organisms. Mitochondrial gene sequence divergence among anthozoan species is also low relative to that exhibited in other animals, although higher level relationships can be resolved with these markers. Substitution rates in anthozoan nuclear genes are much higher than in mitochondrial genes, whereas nuclear genes in other metazoans usually evolve more slowly than, or similar to, mitochondrial genes. Although several mechanisms accounting for a slow rate of sequence evolution have been proposed, there is not yet a definitive explanation for this observation. Slow evolution and unique characteristics may be common in primitive metazoans, suggesting that patterns of mtDNA evolution in these organisms differ from that in other animal systems.     

The evolution of fishes and corals on reefs: form,function and interdependence

Coral reefs are renowned for their spectacular biodiversity and the close links between fishes and corals. Despite extensive fossil records and common biogeographic histories, the evolution of these two key groups has rarely been considered together. We therefore examine recent advances in molecular phylogenetics and palaeoecology, and place the evolution of fishes and corals in a functional context. In critically reviewing the available fossil and phylogenetic evidence, we reveal a marked congruence in the evolution of the two groups. Despite one group consisting of swimming vertebrates and the other colonial symbiotic invertebrates, fishes and corals have remarkably similar evolutionary histories. In the Paleocene and Eocene [66–34 million years ago (Ma)] most modern fish and coral families were present, and both were represented by a wide range of functional morphotypes. However, there is little evidence of diversification at this time. By contrast, in the Oligocene and Miocene (34–5.3 Ma), both groups exhibited rapid lineage diversification. There is also evidence of increasing reef area, occupation of new habitats, increasing coral cover, and potentially, increasing fish abundance. Functionally, the Oligocene–Miocene is marked by the appearance of new fish and coral taxa associated with high‐turnover fast‐growth ecosystems and the colonization of reef flats. It is in this period that the functional characteristics of modern coral reefs were established. Most species, however, only arose in the last 5.3 million years (Myr; Plio–Pleistocene), with the average age of fish species being 5.3 Myr, and corals just 1.9 Myr. While these species are genetically distinct, phenotypic differences are often limited to variation in colour or minor morphological features. This suggests that the rapid increase in biodiversity during the last 5.3 Myr was not matched by changes in ecosystem function. For reef fishes, colour appears to be central to recent diversification. However, the presence of pigment patterns in the Eocene suggests that colour may not have driven recent diversification. Furthermore, the lack of functional changes in fishes or corals over the last 5 Myr raises questions over the role and importance of biodiversity in shaping the future of coral reefs.     

Evolution of the optimal reproductive schedule in the ant Camponotus (Colobopsis) nipponicus (wheeler): a demographic approach

1. Traits are hypothesised to optimise via natural selection. The schedule of reproduction is an important adaptive trait, but its evolution is difficult to study, as measuring parameters is usually difficult. However, the sufficient amounts of demographic data enable us to estimate these parameters. 2. Here, it is shown that the reproductive schedule of the ant Camponotus (Colobopsis) nipponicus is tuned to maximise the lifetime production of alates. 3. A colony started its reproduction 4 years after the colony founding, at which time they were far smaller than well‐developed colonies. This contradicts the prediction of the bang‐bang strategy theory. The size distribution of colonies in the study area showed that the mortality of small colonies is much higher than that of large colonies. 4. A simulation analysis suggests that the colonies that are smaller than the threshold can still achieve significant improvement in colny survival to the following year by investing all resources in colony growth instead of reproduction. A sensitivity analysis for the starting year of reproduction showed that the observed schedule maximises lifetime alate production. The demographic data suggest a stable population, which is required for optimisation through this maximisation. 5. The observed reproductive schedule must be optimised, and the breakdown of the bang‐bang theory is due to higher mortalities during the incipient stage of colonies. This study demonstrates that having enough demographic data creates a useful tool for studying the evolution of life‐history characteristics.     

CO2 enrichment and reduced seawater pH had no effect on the embryonic development of Acropora palmata (Anthozoa,Scleractinia).

The effects of decreased pH, caused by carbon dioxide (CO₂) dissolution in seawater (known as ocean acidification (OA)), on the development of newly fertilized eggs of the Caribbean reef-building coral, Acropora palmata, was tested in three experiments conducted during the summers of 2008 and 2009 (two repeats). Three levels of CO₂ enrichment were used: present day conditions (400?µatm, pH 8.1) and two CO₂-enriched conditions (700?µatm, pH 7.9, and 1000?µatm, pH 7.7). No effects on the progression or timing of development, or embryo and larval size, were detected in any of the three experimental runs. The results show that the embryos and larvae of A. palmata are able to develop normally under seawater pH of at least 0.4 pH units lower than the present levels. Acropora palmata larvae do not usually begin to calcify after settlement, so this study only examined the non-calcifying part of the life cycle of this species. Most of the concern about the effects of OA on marine organisms centers on its effect on calcification. Negative effects of OA on the embryonic development of this species were not found and they may not manifest until the newly settled polyps begin to calcify.     

Age‐based demographic and reproductive assessment of orangespine Naso lituratus and bluespine Naso unicornis unicornfishes

Bluespine unicornfish Naso unicornis and orangespine unicornfish Naso lituratus were sampled in Pohnpei and Guam, Micronesia, over 13 months to identify reproductive and age‐based demographic features necessary for informed management. Age and reproductive information were derived from analysis of sagittal otoliths and gonads. Both species had moderate life spans [maximum ages of 23 (N. unicornis) and 14 years (N. lituratus)] compared with published estimates of conspecifics from other locations (>30 years) and of other Naso species. Length at maturation for N. unicornis was similar between Pohnpei and Guam while females consistently matured at a larger size [c. 30 cm fork length (L_F)] than males (c. 27 cm L_F). This sex‐specific pattern was reversed in N. lituratus for which estimates of maturation length (females: 15 cm L_F; males: 18 cm L_F) were only obtained from Guam. Developmental patterns in female gonads of both species suggested that initiation of maturation occurs very early. Growth patterns of N. lituratus displayed rapid asymptotic growth compared with N. unicornis and other congeners as well as slight sex‐specific patterns of length‐at‐age. Results highlight the considerable spatial variation that may occur in the population biology of these species across various scales. Additionally, proper management remains complicated without improved knowledge of fishery trends and reproductive behaviour in unicornfishes, species that are prime fishery targets in Micronesia and elsewhere.     

Mechanical vulnerability explains size‐dependent mortality of reef corals

Understanding life history and demographic variation among species within communities is a central ecological goal. Mortality schedules are especially important in ecosystems where disturbance plays a major role in structuring communities, such as coral reefs. Here, we test whether a trait‐based, mechanistic model of mechanical vulnerability in corals can explain mortality schedules. Specifically, we ask whether species that become increasingly vulnerable to hydrodynamic dislodgment as they grow have bathtub‐shaped mortality curves, whereas species that remain mechanically stable have decreasing mortality rates with size, as predicted by classical life history theory for reef corals. We find that size‐dependent mortality is highly consistent between species with the same growth form and that the shape of size‐dependent mortality for each growth form can be explained by mechanical vulnerability. Our findings highlight the feasibility of predicting assemblage‐scale mortality patterns on coral reefs with trait‐based approaches.     

Sexual reproduction in three hermaphroditic deep-sea Caryophyllia species (Anthozoa: Scleractinia) from the NE Atlantic Ocean

The reproductive biology and gametogenesis of three species of Caryophyllia were examined using histological techniques. Caryophyllia ambrosia, Alcock 1898, C. cornuformis, Pourtales 1868, and C. sequenzae, Duncan 1873, were collected from the Porcupine Seabight and Rockall Trough in the NE Atlantic Ocean. These three ahermatypic solitary corals inhabit different depth ranges: C. cornuformis – 435–2000 m, C. sequenzae – 960–1900 m, and C. ambrosia – 1100–3000 m. All three species are hermaphroditic. Hermaphroditism in these species was found to be cyclical, with only one sex of gametes viable in any individual at any point in time, although gametes of both sexes were found together within a single mesentery. Once the viable gametes are spawned, the next sex of gametes continues to grow until mature, and so gametogenesis is a continuous cycle. Oocytes and spermacysts in all species increased in density towards the actinopharynx. Maximum fecundity for C. sequenzae was 940 oocytes per polyp, and for C. ambrosia 2900 oocytes per polyp. Fecundity could not be established for C. cornuformis. In all three species, individuals were asynchronous within populations, and production of gametes was quasi-continuous throughout the year. All species are hypothesised to have lecithotrophic larvae owing to their large oocyte sizes (C. cornuformis max – 350 μm; C. sequenzae max – 430 μm; C. ambrosia max – 700 μm). Both the average oocyte size and fecundity increased in species going down the depth gradient of the NE Atlantic.     

Influence of different substrates on the evolution of morphology and life‐history traits of azooxanthellate solitary corals (Scleractinia: Flabellidae)

Sessile organisms are influenced considerably by their substrate conditions, and their adaptive strategies are key to understanding their morphologic evolution and traits of life history. The family Flabellidae (Cnidaria: Scleractinia) is composed of the representative azooxanthellate solitary corals that live on both soft and hard substrates using various adaptive strategies. We reconstructed the phylogenetic tree and ancestral character states of this family from the mitochondrial 16S and nuclear 28S ribosomal DNA sequences of ten flabellids aiming to infer the evolution of their adaptive strategies. The Javania lineage branched off first and adapted to hard substrates by using a tectura‐reinforced base. The extant free‐living flabellids, including Flabellum and Truncatoflabellum, invaded soft substrates and acquired the flabellate corallum morphology of their common ancestor, followed by a remarkable radiation with the exploitation of adaptive strategies, such as external soft tissue [e.g. Flabellum (Ulocyathus)], thecal edge spine, and transverse division (e.g. Placotrochus and Truncatoflabellum). Subsequently, the free‐living ancestors of two genera (Rhizotrochus and Monomyces) invaded hard substrates independently by exploiting distinct attachment apparatuses such as tube‐like and massive rootlets, respectively. In conclusion, flabellids developed various morphology and life‐history traits according to the differences in substrate conditions during the course of their evolution. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 184–192.     

Life history evolution in cichlids 2: directional evolution of the trade-off between egg number and egg size

The negative relationship between offspring number and offspring size provides a classic example of the role of trade-offs in life history theory. However, the evolutionary transitions in egg size and clutch size that have produced this negative relationship are still largely unknown. Since body size may affect both of these traits, it would be helpful to understand how evolutionary changes in body size may have facilitated or constrained shifts in clutch and egg size. By using comparative methods with a database of life histories and a phylogeny of 222 genera of cichlid fishes, we investigated the order of evolutionary transitions in these traits in relation to each other. We found that the ancestral large-bodied cichlids first increased egg size, followed by a decrease in both body size and clutch size resulting in the common current combination of a small-bodied cichlid with a small clutch of large eggs. Furthermore, lineages that deviated from the negative relationship between clutch and egg size underwent different transitions in these traits according to their body size (large bodied genera have moved towards the large clutch/small egg end of the continuum and small bodied genera towards the small clutch/large egg end of the continuum) to reach the negative relationship between clutch size and egg size. Our results show that body size is highly important in shaping the negative relationship between clutch size and egg size.     

Deltocyathiidae,an early‐diverging family of Robust corals (Anthozoa,Scleractinia)

Kitahara, M.V., Cairns, S.D., Stolarski, J. & Miller, D.J. (2012). Deltocyathiidae, an early‐diverging family of Robust corals (Anthozoa, Scleractinia). —Zoologica Scripta, 00, 000–000. Over the last decade, molecular phylogenetics has called into question some fundamental aspects of coral systematics. Within the Scleractinia, most families composed exclusively by zooxanthellate species are polyphyletic on the basis of molecular data, and the second most speciose coral family, the Caryophylliidae (most members of which are azooxanthellate), is an unnatural grouping. As part of the process of resolving taxonomic affinities of ‘caryophylliids’, here a new ‘Robust’ scleractinian family (Deltocyathiidae fam. n.) is proposed on the basis of combined molecular (CO1 and 28S rDNA) and morphological data, accommodating the early‐diverging clade of traditional caryophylliids (represented today by the genus Deltocyathus). Whereas this family captures the full morphological diversity of the genus Deltocyathus, one species, Deltocyathus magnificus, is an outlier in terms of molecular data, and groups with the ‘Complex” coral family Turbinoliidae. Ultrastructural data, however, place D. magnificus within Deltocyathiidae fam. nov. Unfortunately, limited ultrastructural data are as yet available for turbinoliids, but D. magnificus may represent the first documented case of morphological convergence at the microstructural level among scleractinian corals. Marcelo V. Kitahara, Centro de Biologia Marinha, Universidade de São Paulo, São Sebastião, S.P. 11600‐000, Brazil. E‐mail: kitahara@usp.br     

Electrophoretic identification of poritid species (Anthozoa: Scleractinia)

Electrophoretic surveys of 13 enzyme-coding loci distinguished unambiguously five morphologically defined species of Porites and two species of Goniopora. Each species was identifiable solely by unique, qualitative banding patterns at 1–6 loci. Genetic distances give preliminary estimates that these Porites species diverged from common ancestors 8–22 Ma during the Miocene, and that the two Goniopora species diverged about 3.5 Ma in the Pliocene, assuming Porites evolved from Goniopora 55 million years ago (Ma). Correspondence to: R. L. Garthwaite     

Correlated evolution of conspicuous coloration and body size in poison frogs (Dendrobatidae)

Conspicuous coloration is often used in combination with chemical defenses to deter predators from attacking. Experimental studies have shown that the avoidance inducing effect of conspicuous prey coloration increases with increasing size of pattern elements and with increasing body size. Here we use a comparative approach to test the prediction from these findings, namely that conspicuous coloration will evolve in tandem with body size. In our analysis, we use a previously published mitochondrial DNA-based phylogeny and comparative analysis of independent contrasts to examine if evolutionary shifts in color pattern have been associated with evolutionary changes in body size in aposematic poison frogs (Anura: Dendrobatidae). Information on body size (snout to vent length) and coloration were obtained from the literature. Two different measures of conspicuousness were used, one based on rankings by human observers and the other based on computer analysis of digitized photographs. The results from comparative analyses using either measure of coloration indicated that avoidance inducing coloration and body size have evolved in concert in poison frogs. Results from reconstruction of character change further indicate that the correlated evolution of size and coloration has involved changes in both directions within each of the different clades of the phylogenetic tree. This finding is consistent with the hypothesis that selection imposed by visually guided predators has promoted the evolution of larger body size in species with conspicuous coloration, or enhanced evolution of conspicuous coloration in larger species.     

Host choice and fitness of anemonefish Amphiprion ocellaris (Perciformes: Pomacentridae) living with host anemones (Anthozoa: Actiniaria) in captive conditions

In this study, we investigated the host choice of naïve Amphiprion ocellaris, a specialist, at two different stages of development (newly settling juveniles and post-settlement juveniles). The fish were exposed to their natural and unnatural host species in the laboratory and their fitness was assessed in terms of activity and growth rate. Newly settling juveniles exhibited little host preference, while post-settlement juveniles immediately associated with their most common host in the wild. The analysis of fish activity confirmed that A. ocellaris is diurnal; they are most active in the morning, less at midday and barely move at night. The average travelling distance of juveniles was shorter in the groups living with their natural host, increasing in the groups living with an unnatural host and was highest in groups that did not become associated with any other unnatural host species. Post-settlement juveniles living with the natural host species grew better than those living with unnatural hosts or without anemone contact. These results suggest that the welfare of A. ocellaris in captivity will be optimized by keeping them with their natural anemone host species, although more generalist Amphiprion species may survive in association with other hosts.     

Photosynthetic activity of a temperate coral Acropora pruinosa (Scleractinia, Anthozoa) with symbiotic algae in Japan

Physiological properties of the temperate hermatypic coral Acropora pruinosa Brook with symbiotic algae (zooxanthellae) on the southern coast of the Izu Peninsula, Shizuoka Prefecture, central Japan, were compared between summer and winter. Photosynthesis and respiration rates of the coral with symbiotic zooxanthellae were measured in summer and winter under controlled temperatures and irradiances with a differential gasvolumeter (Productmeter). Net photosynthetic rate under all irradiances was higher in winter than in summer at the lower range of temperature (12–20°C), while lower than in summer at the higher range of temperature (20–30°C). The optimum temperature for net photosynthesis was apt to fall with the decrease of irradiance both in summer and winter, whereas it was higher in summer than in winter under each irradiance. At 25/ 50/100 μmol photons nr² s^?1, it was nearly the sea‐water temperature in each season. Dark respiration rate was higher in winter than in summer, especially in the range from 20–30°C. In both seasons the optimum temperature for gross photosynthesis was 28°C under 400 μmol photons nr² s^?1 and lowered with decreasing irradiance up to 22°C under 25 μmol photons nr² s^?1 in summer, while 20°C under the same irradiance in winter. The optimum temperature for production/respiration (P/R) ratio was higher in summer than in winter under each irradiance. Results indicated that metabolism of coral and zooxanthellae is adapted to ambient temperature condition under nearly natural irradiance in each season.     

Correlated evolution of female neoteny and flightlessness with male spermatophore production in fireflies (Coleoptera: Lampyridae)

The beetle family Lampyridae (fireflies) encompasses ～100 genera worldwide with considerable diversity in life histories and signaling modes. Some lampyrid males use reproductive accessory glands to produce spermatophores, which have been shown to increase female lifetime fecundity. Sexual dimorphism in the form of neotenic and flightless females is also common in this family. A major goal of this study was to test a hypothesized link between female flight ability and male spermatophore production. We examined macroevolutionary patterns to test for correlated evolution among different levels of female neoteny (and associated loss of flight ability), male accessory gland number (and associated spermatophore production), and sexual signaling mode. Trait reconstruction on a molecular phylogeny indicated that flying females and spermatophores were ancestral traits and that female neoteny increased monotonically and led to flightlessness within multiple lineages. In addition, male spermatophore production was lost multiple times. Our evolutionary trait analysis revealed significant correlations between increased female neoteny and male accessory gland number, as well as between flightlessness and spermatophore loss. In addition, female flightlessness was positively correlated with the use of glows as female sexual signal. Transition probability analysis supported an evolutionary sequence of female flightlessness evolving first, followed by loss of male spermatophores. These results contribute to understanding how spermatophores have evolved and how this important class of seminal nuptial gifts is linked to other traits, providing new insights into sexual selection and life-history evolution.     

Bidirectional sex change in mushroom stony corals

Sex change occurs when an individual changes from one functional sex to another. The direction of sex change occurs mainly from male to female (protandry) or vice versa (protogyny), but sometimes may be bidirectional (repetitive). Here, for the first time in stony corals, we report on a protandrous sex change exhibited by two mushroom corals, Fungia repanda and Ctenactis echinata, with the latter also exhibiting bidirectional sex change. Compared with C. echinata, F. repanda exhibited relatively earlier sex change, significantly slower growth and higher mortality rates, in accordance with sex-allocation theory. Sex ratio in both the species was biased towards the first sex. The bidirectional sex change displayed by C. echinata greatly resembles that of dioecious plants that display labile sexuality in response to energetic and/or environmental constraints. We posit that, similar to these plants, in the studied corals, sex change increases their overall fitness, reinforcing the important role of reproductive plasticity in scleractinian corals in determining their evolutionary success.