Correlated evolution of sex and reproductive mode in corals (Anthozoa: Scleractinia)

Sexuality and reproductive mode are two fundamental life-history traits that exhibit largely unexplained macroevolutionary patterns among the major groups of multicellular organisms. For example, the cnidarian class Anthozoa (corals and anemones) is mainly comprised of gonochoric (separate sex) brooders or spawners, while one order, Scleractinia (skeleton-forming corals), appears to be mostly hermaphroditic spawners. Here, using the most complete phylogeny of scleractinians, we reconstruct how evolutionary transitions between sexual systems (gonochorism versus hermaphrodism) and reproductive modes (brooding versus spawning) have generated large-scale taxonomic patterns in these characters. Hermaphrodites have independently evolved in three large, distantly related lineages consisting of mostly reef-building species. Reproductive mode in corals has evolved at twice the rate of sexuality, while the evolution of sexuality has been heavily biased: gonochorism is over 100 times more likely to be lost than gained, and can only be acquired by brooders. This circuitous evolutionary pathway accounts for the prevalence of hermaphroditic spawners among reef-forming scleractinians, despite their ancient gonochoric heritage.     

Mass brooding of the blue octocoral,Heliopora coerulea on a sedimented equatorial reef

The octocoral Heliopora coerulea is a gonochoric surface brooder. Although the species is common on shallow Indo-Pacific coral reefs, information on its reproductive biology is limited and spawning timings have only been reported from four locations. We report the first observations of surface brooding in H. coerulea on a sedimented equatorial reef. In April 2014, 46 and 26 brooding colonies were recorded, respectively, from reefs fringing the islands of Kusu and Lazarus in Singapore. The brooded coral larvae were tightly bound to inflated coral polyps, forming a dense white mat which blanketed the brown coral tissue. The inflated polyps also protruded from layers of sediment, which accumulated in colony crevices, such that the brooded larvae were elevated above the settled sediment. Our observations supplement existing knowledge on the reproductive timing of H. coerulea and highlight the adaptations that improve survival of this species on sediment-impacted reefs.     

Unusual pattern of embryogenesis of Caryophyllia inornata (scleractinia,caryophylliidae) in the mediterranean sea: Maybe agamic reproduction?

While knowledge of the reproductive biology of tropical scleractinian corals is extensive, information from temperate zones is limited. The aim of this study is to describe the reproductive biology of Caryophyllia inornata, a temperate species, and to increase the understanding of the reproductive strategies of Mediterranean corals. Samples of C. inornata were collected during SCUBA surveys at Elba island. Sexually active individuals displayed either male or female germ cells, showing a gonochoric sexuality. C. inornata exhibited an unusual pattern of embryogenesis. Embryos appeared throughout the whole year in males and in sexually inactive individuals, and they did not show a seasonal pattern of development, as usually expected for sexual reproduction. This observation suggests the possibility of asexual origin. These embryogenetic sexually inactive individuals were larger in size than the embryogenetic sexually active ones, and they might be senile polyps that preserve the ability to produce embryos only by agamic reproduction. J. Morphol. 2012. © 2012 Wiley Periodicals, Inc.     

Comparisons of sexual reproduction in Carijoa riisei (Cnidaria,Alcyonacea) in South Atlantic,Caribbean, and Pacific areas

Soft corals show a wide variety of reproductive strategies, including both asexual and sexual reproduction which can influence macro-evolutionary processes. The octocoral Carijoa riisei has an ample geographical distribution in Pacific and southern Atlantic and also in Caribbean region. This species was considered invasive in Hawaii, and its capacity for rapid proliferation is recognized, but recent studies, however, have indicated that it appears to be native to the Indo-Pacific region. The present study examined the reproductive biology of C. riisei in the Atlantic basin. The results were then compared to previous studies of the same species from the Pacific (Hawaii) and Caribbean (Puerto Rico) regions to examine the hypothesis that the reproductive patterns of C. riisei populations are the same throughout its geographical distribution, independent of its native or non-native status. Samples were collected on a monthly basis from May/2007 to April/2008 at Porto de Galinhas (Pernambuco State, Brazil). This species was found to have similar reproduction patterns in Brazil, the Caribbean, and in Hawaii (a gonochoric reproductive pattern and continuous and asynchronous gamete release). The similarities of their traits contribute to its rapid proliferation and occupation of spaces left by other species, independent of its native or non-native status.     

Reproduction of the gorgonian Plexaura flexuosa in Bermuda

This study examined geographically based differences in reproductive biology of Plexaura flexuosa, a gonochoric broadcasting gorgonian that is abundant across the tropical and subtropical Western Atlantic. Gametogenesis, spawning, and per polyp fecundity-colony height ratios were assessed in Bermuda and then compared with existing studies of populations in the Bahamas, Florida, and the Caribbean and in conjunction with analyses of mean sea surface temperature (MSST) at these locales. Differences documented in the Bermudian population include: lag in onset of spermary development and completion of oogenesis as compared to southern populations; later spawning that occurred over fewer days; and lack of correlation between fecundity polyp^− 1 and colony height. These findings suggest that important differences occur in major reproductive events between the distantly separated northern-most populations of P. flexuosa found in Bermuda compared with more tropical populations of this species. Such population-level variability in life history characteristics needs to be incorporated into approaches for conservation planning efforts.     

Phenology of sexual reproduction in the common coral reef sponge,Carteriospongia foliascens

Understanding processes that contribute to population maintenance is critical to the management and conservation of species. Despite this, very little is currently known about the reproductive biology of Great Barrier Reef (GBR) sponge species. Here, we established reproductive parameters including mode of sexuality and development, seasonality, sex ratios, gametogenesis, reproductive output, and size at sexual maturity for the common phototrophic intertidal sponge, Carteriospongia foliascens, in the central GBR over two reproductive cycles. A population sexual productivity index (PoSPi) integrating key reproductive parameters was formulated to compare population larval supply over time. This study shows that C. foliascens is reproductive all year round, gonochoric and viviparous, with larvae developing asynchronously throughout the mesohyl. The influence of environmental parameters relevant to C. foliascens reproduction [i.e., sea surface temperature (SST), photoperiod, and rainfall] was also examined, and SST was found to have the most significant effect on phenology. C. foliascens reproduction exhibited annual mono-cyclic patterns closely resembling SST fluctuations. Reproductive output was depressed at low SST (<23 °C) and increased at temperatures above 23 °C. Peak sperm release occurred at temperatures above 25 °C, while peak larval release occurred during the annual temperature maxima (>28 °C). A twofold increase in maximum larval production (PoSPi) in C. foliascens was observed in the second reproductive cycle, following a depressed PoSPi in the first cycle. This reduction in PoSPi in the first reproductive cycle was associated with elevated SST and rainfall, coinciding with one of the strongest La Niña events on record.     

The composition and structure of a protected coral reef in Cam Ranh Bay in the South China Sea

A nonstructural reef at Hon Nai Island in Cam Ranh Bay (southern Vietnam) was investigated. In comparison with most of the coastal continental and island coral reefs of this region, it is characterized by high species richness of reef-building corals, among them scleractinians. A total of 34 species of Acropora were found, which represent 80% of the total species composition of this scleractinian genus on the reefs of Vietnam and 25% on the reefs of the Indo-Pacific. Among 169 species of scleractinians found on the reef of Hon Nai, Favia sp. nov. was previously unknown to science. The vertical bionomic zonality of the reef corresponds to a zonal distribution of environmental factors and is similar to that on reefs of the Gulf of Siam and various areas of the Pacific and the Caribbean Basin. The thriving of the Hon Nai island reef may be connected with protective measures undertaken by the Government of Vietnam and the minimization of anthropogenic impacts due to the activities of the Sanest Co.     

Insights on the female reproductive system in Hippolyte inermis (Decapoda,Caridea): is this species really hermaphroditic?

Abstract. The majority of the published data about the reproductive biology of the decapod shrimp, Hippolyte inermis support the idea that this species is a protandric hermaphrodite, as is reported to be the case for certain other caridean species. However, our studies, based on the relative growth of the male reproductive appendage and histological examinations of the ovary, testes, oviducts, and deferentia vasa, indicate that there is no evidence supporting the occurrence of protandry. The first report of anomalies in the process of sexual inversion is credited to Reverberi (1950) ; however, we have obtained no evidence to support this phenomenon in H. inermis . We have not found either ovotestes or testes transforming into ovotestes. Therefore, we propose that H. inermis is a gonochoric species.     

The reproductive biology and early life ecology of a common Caribbean brain coral, <Emphasis Type="Italic">Diploria labyrinthiformis</Emphasis> (Scleractinia: Faviinae)

Despite the fact that most of the severe demographic bottlenecks in coral populations occur during their earliest life stages, information on the reproductive biology and early life history traits of many coral species is limited and often inferred from adult traits only. This study reports on several atypical aspects of the reproductive biology and early life ecology of the grooved brain coral, Diploria labyrinthiformis (Linnaeus, 1758), a conspicuous reef-building species on Caribbean reefs. The timing of gamete release of D. labyrinthiformis was monitored in Curaçao over eight consecutive months, and embryogenesis, planulae behavior, and settlement rates were observed and quantified. We further studied growth and symbiont acquisition in juvenile D. labyrinthiformis for 3.5 yr and compared settler survival under ambient and nutrient-enriched conditions in situ. Notably, D. labyrinthiformis reproduced during daylight hours in six consecutive monthly spawning events between May and September 2013, with a peak in June. This is the largest number of reproductive events per year ever observed in a broadcast-spawning Caribbean coral species. In settlement experiments, D. labyrinthiformis planulae swam to the bottom of culture containers 13 h after spawning and rapidly settled when provided with settlement cues (42% within 14 h). After 5 months, the survival and growth rates of settled juveniles were 3.7 and 1.9 times higher, respectively, for settlers that acquired zooxanthellae within 1 month after settlement, compared to those that acquired symbionts later on. Nutrient enrichment increased settler survival fourfold, but only for settlers that had acquired symbionts within 1 month after settlement. With at least six reproductive events per year, a short planktonic larval phase, high settlement rates, and a positive response to nutrient enrichment, the broadcast-spawning species D. labyrinthiformis displays a range of reproductive and early life-history traits that are more often associated with brooding coral species, illustrating that classical divisions of coral species by reproductive mode alone do not always reflect the true biology and ecology of their earliest life stages.     

Reproductive ecology of Caribbean reef corals

The last decade has seen a resurgence of interest in the processes of sexual reproduction by scleractinian reef corals. Earlier investigations had focused fortuitously on brooding (planulating) species, which resulted in the general misconception that brooding was the main form of larval development of reef corals. More recent work on Indo-Pacific species has shown broadcast spawning and short annual reproductive periods to predominate. This report presents the reproductive patterns of eleven Caribbean coral species and attempts to explain the adaptive features and selective pressures that have led to the evolution of the four reproductive patterns described to date: (a) hermaphroditic broadcasters; (b) gonochoric broadcasters; (c) hermaphroditic broadcasters; (b) gonochoric brooders. Both (a) and (b) correlate with large colony size and short annual spawning periods; and (c) and (d) correlate with small colony size, multiple planulating cycles per year, and occupation of unstable habitats. Selection for outcrossing between long-lived individuals is proposed as the reason for gonochorism and for synchronous spawning of hermaphroditic broadcasters, and also for the large amount of sperm produced by hermaphroditic brooders. Selection for high rates of local recruitment is proposed as the force behind the evolution of brooding by species inhabiting unstable habitats and suffering high rates of adult mortality.     

An aquarium experiment for identifying the physical factors inducing morphological change in two massive scleractinian corals

Previous research has demonstrated that the massive corals Favia speciosa (Dana, 1846) and Diploastrea heliopora (Lamark, 1816) are phenotypically plastic, i.e. the phenotype of these species can be altered by environmental conditions within their life span. Many researchers have suggested that light, water movement and/or sediment can affect coral morphology, but no work to date has attempted to separate these variables in a controlled aquarium experiment. To ascertain whether any of these three factors could induce morphological change in F. speciosa and D. heliopora, fragments (clone-mates) of both species were maintained in five aquarium tanks, representing: high water energy, high sedimentation, and three different light regimes. After 4 months, the architecture of 12 randomly chosen corallites from each fragment was measured. Reaction norms suggest a relationship between corallite morphology and light, but no consistent pattern could be detected for fragments kept in the sediment regime tank or the high water energy tank. Corallites expand, extend and deepen in high light conditions and possible functional explanations for this response are presented. However, more research is necessary to confirm that light is the primary controlling factor inducing small-scale morphological change in F. speciosa and D. heliopora.     

Changes in the composition and structure of coral communities of Mju and Moon islands, Nha Trang Bay, South China Sea

In October 2003 and January 2005, comparative observations were made on the reefs of Mju and Moon islands near the city and port of Nha Trang, which we first investigated in 1981. Appreciable changes due to anthropogenic impact have occurred on the reefs that are the nearest to the city. There was a reduction in substrate cover by reef-building corals, a substitution of dominant scleractinian species, and a decrease in the numbers and diversity of common species of corallobionts. The index of species diversity for scleractinians also decreased. The seaweeds Chnoospora and Halimeda spread into all zones of the reefs. Changes in coral communities on more distant and protected reefs were not so marked.     

Reproductive biology, development, and planula behavior in the Caribbean gorgonian Pseudopterogorgia elisabethae

Abstract. The reproductive biology, development, and planula behavior of the gorgonian Pseudopterogorgia elisabethae were studied at 2 sites in the Bahamas between 1996 and 2001. Colonies were gonochoric, and females brooded planulae on the colony surface. Gonads were observed only in colonies 18 cm high or larger. Spawning was asynchronous within and between sites but was concentrated 2–10 days after the new moons from late November through early January. Fertilized eggs developed into planulae over 1–2 days and the planulae remained attached to the surface of the female colony for an additional 2–4 days. Planulae were negatively buoyant and field observations suggest that larvae may settle within tens of meters of the maternal colony. P. elisabethae is harvested for natural products, and information on the reproduction of this commercially important species is crucial to the understanding of its population biology and to the development of management plans for the conservation of the species.     

The reproductive system of Hippolyte niezabitowskii (Decapoda, Caridea)

Data on the reproductive biology of the genus Hippolyte are available from studies of Hippolyte inermis. These findings support the idea that these species are protandric hermaphrodites, exhibiting sex reversal. However, recent studies of this and other species, such as Hippolyte obliquimanus and Hippolyte williamsi, have not reported sex reversal and suggest a gonochoric condition. In the present study, histological analyses were conducted of the ovaries, testes, oviducts, vasa deferentia and the development of the male appendage. The results of this study show that the Hippolyte niezabitowskii population from southern Spain should also be viewed as a gonochoric species. The study found no evidence of sex reversals. These conclusions are also supported by information on the structure of the population and by the results of studies of the male appendage. The population structure involves different size distributions of males and of females. Size classes 2-14 exhibit substantial overlap. No evidence of sex reversal was obtained from the study of the male appendage.     

Characterization of the complete mitochondrial genome of Diploastrea heliopora and phylogeny of the scleractinia species which have group I introns in their COI genes

Mitochondrial genome DNA is a powerful marker for resolving phylogenetic relationships among scleractinian corals. Here, we decode the complete mitochondrial genome of Diploastrea heliopora (Lamarck, 1816) for the first time. The general features are 18 363 bp in length, and conventionally, with 13 protein coding genes, two ribosomal RNAs, and two transfer RNAs. Gene arrangement and distribution are similar to other scleractinian corals. Moreover, the COI gene of D. heliopora is broken up into two parts by a complex group I intron. This intron is 1076 bases in length and contains helical structures (P1-P10, except P2) and four conserved regions (P, Q, R, and S). The mitochondrial genome of D. heliopora has asymmetric base composition (13.03% C, 20.29% G, 25.91% A, and 40.77% for T). Based on concatenated protein coding genes, ML and BI trees show similar phylogenetic relationship: D. heliopora clustered closely with Sclerophyllia maxima and Echinophyllia aspera into the robust branch. The data and conclusion in this study are reference for further phylogenetic studies of corals.     

Sexual reproduction of Hawaiian black corals,with a review of the reproduction of antipatharians (Cnidaria: Anthozoa: Hexacorallia)

Abstract. Black corals (Cnidaria: Antipatharia) are ecologically important members of the sessile invertebrate fauna, but due to their typical deep‐water environments (>50 m), very little is known about their basic biology, including reproduction. We used histological techniques to examine the sexual reproduction of members of eight species of antipatharians collected from the Hawaiian Islands over a wide depth range (10–1327 m). Gametes of all species examined were found in association with the primary transverse mesenteries, which in some cases reached into the cavity of lateral tentacles. Specimens contained either spermatocysts or oocytes, but never both within the same individual, suggesting either a gonochoric or a sequentially hermaphroditic mode of reproduction. No developing embryos or larvae were observed in any of the samples, indicating that fertilization and larval development likely occur externally in the water column and not internally within polyps. We compared our results with previously published information on the sexual reproduction of antipatharians. Our review suggests that in antipatharians, more generally, (1) entire colonies are either female or male (although sequential hermaphroditism cannot be ruled out in most cases and has been reported previously for one species), (2) gametes are confined to the primary transverse mesenteries in most species, and (3) there is no evidence of internal fertilization. Further studies are needed to determine whether gonochorism or sequential hermaphroditism is more prevalent within the Antipatharia, whether dimorphic polyps occur within this taxonomic order, and to examine the reproductive seasonality and larval behavior of individual species.     

Cycle of gonadal development in Eunicella singularis (Cnidaria: Octocorallia): trends in sexual reproduction in gorgonians

Abstract. Eunicella singularis is a gorgonian species whose members are abundant in hard-bottom sublittoral communities of the Mediterranean Sea. The reproductive biology in this species has been examined to better understand the ability in this species to recover from recent mass mortality events. Eunicella singularis is a stable, gonochoric, iteroparous species that reproduces annually and exhibits a seasonal pattern of gametogenesis characterized by a single annual maturation of the gametes. The sex ratio did not significantly differ from 1:1. Oogenesis lasted 13–17 months, beginning between February and June, and ending with the release of 0.7 planula larvae per polyp between late May and July of the following year. The diameter of mature oocytes ranged 450–860 μm. Spermatogenesis was much shorter than oogenesis and occurred over 5–6 months. Gonadal production of both sexes increased in spring and culminated with the spawning of male colonies in late May–June. Fertilization of oocytes and development of the planula larvae occurred within the polyps of female colonies. Planula release was observed in June and July. The patterns emerging from this and previous studies on sexual reproduction of Mediterranean gorgonians suggest that investment in gonad development appears to be related to resource availability.     

Intraspecific sperm competition genes enforce post-mating species barriers in Drosophila

Sexual selection and sexual conflict are considered important drivers of speciation, based on both theoretical models and empirical correlations between sexually selected traits and diversification. However, whether reproductive isolation between species evolves directly as a consequence of intrapopulation sexual dynamics remains empirically unresolved, in part because knowledge of the genetic mechanisms (if any) connecting these processes is limited. Here, we provide evidence of a direct mechanistic link between intraspecies sexual selection and reproductive isolation. We examined genes with known roles in intraspecific sperm competition (ISC) in D. melanogaster and assayed their impact on conspecific sperm precedence (CSP). We found that two such genes (Acp36DE and CG9997) contribute to both offensive sperm competition and CSP; null/knockdown lines both had lower competitive ability against D. melanogaster conspecifics and were no longer able to displace heterospecific D. simulans sperm in competitive matings. In comparison, Sex Peptide (Acp70A)—another locus essential for ISC—does not contribute to CSP. These data indicate that two loci important for sperm competitive interactions have an additional role in similar interactions that enforce post-mating reproductive isolation between species, and show that sexual selection and sexual isolation can act on the same molecular targets in a gene-specific manner.     

Sperm morphology of scleractinians from the Caribbean

This study compares the sperm morphology of 2 hermaphroditic (Diploria strigosa, Montastrea annularis) and 2 gonochoric (Siderastrea siderea, Dendrogyra cylindrus) Caribbean reef corals. The spermatozoa of the gonochoric species are morphologically more specialized than those of the hermaphrodites. The cytological differences are apparent in the formation of a Spitzenkörper and pro-acrosomal vesicles, a mitochondrial mass (Nebenkern) and a large lipid vesicle in the gonochorists studied. Harrison (1985) first demonstrated that sperm morphology is correlated with sexual reproductive pattern and systematic position in scleractinian corals, and this is supported by the results of this study. The possible functional and phylogenetic bases of sperm morphology are discussed and a brief outline is given of further studies required.