Simultaneous Hermaphrodites Research Articles

Genetic variation in the brooding brittle-star: a global hybrid polyploid complex?

The widespread and abundant brooding brittle-star (Amphipholis squamata) is a simultaneous hermaphrodite with a complex mitochondrial phylogeography of multiple divergent overlapping mtDNA lineages, high levels of inbreeding or clonality and unusual sperm morphology. We use exon-capture and transcriptome data to show that the nuclear genome comprises multiple (greater than 3) divergent (π > 6%) expressed components occurring across samples characterized by highly divergent (greater than 20%) mitochondrial lineages, and encompassing several other genera, including diploid dioecious species. We report a massive sperm genome size in A. squamata, an order of magnitude larger than that present in other brittle-stars, and consistent with our SNP-based measure of greatly elevated ploidy. Similarity of these genetic signatures to well-known animal systems suggests that A. squamata (and related taxa) is a hybrid polyploid asexual complex of variable subgenome origins, ploidy and reproductive mode. We discuss enigmatic aspects of A. squamata biology in this light. This putative allopolyploid complex would be the first to be reported from the phylum Echinodermata.

The Complete Genome Sequences of 7 Hypoplectrus species (Serranidae, Perciformes).

Species in the genus Hypoplectrus are found primarily in coral reefs in the Caribbean Sea and the Gulf of Mexico, particularly around Florida and the Bahamas. They are a popular choice for hobbyist saltwater aquariums. Members of this genus are simultaneous hermaphrodites, as they have both male and female sexual organs at the same time as an adult. We present the genome sequences of 7 species of Hypoplectrus. Raw read data and assembled genomes are available in Genbank.

Sublethal heat reduces overall reproductive investment and male allocation in a simultaneously hermaphroditic snail species.

The exposure to sublethally high temperature reduces reproductive performance in diverse organisms. Although this effect has been particularly emphasized for males or male reproductive functioning, it remains largely unknown whether the effect of heat on fertility is sex-specific. Here we examined the impact of sublethally high temperature on male and female functions in a simultaneously hermaphroditic snail species, Lymnaea stagnalis. Examining hermaphrodites is useful to evaluate the sex-specific impacts of heat exposure, since they possess male and female functions within a single individual, sharing genetic and environmental factors. Moreover, previously developed sex allocation theory allows us to compare the differential performance of sex functions. In this study, we exposed snails to 20°C (control), 24°C and 28°C for 14 days and assessed their egg and sperm production, sperm transfer, mating behaviour and growth. Both types of gamete production were significantly reduced by higher temperature, leading to an overall reduction of reproductive investment. By quantifying sex allocation, we furthermore revealed that the heat-stressed snails reduced the relative investment in their male function. This study illustrates that examining simultaneous hermaphrodites can provide significant insights for the impact of heat, and the proximate mechanism, on reproduction in diverse organisms.

Mating roles, copulation duration and reproductive output in the hermaphroditic freshwater snail Planorbella trivolvis

ABSTRACT Hermaphrodites exhibit a wide variety of reproductive strategies, yet empirical studies lag behind theories about their evolution. Planorbella trivolvis, a simultaneous hermaphrodite capable of reciprocal copulation and rare self-fertilization, provides a unique model system for studying reproduction. This study assessed sex roles during mating, demonstrating that mating is primarily reciprocal, and investigated the relationship between physical coupling and reproductive output for single copulation events. Snails were isolated before sexual maturity and placed in 10-l aquaria in size-matched groups. Upon copulation, pairs were removed to small cups until they separated; they were then kept isolated and eggs counted until egg production ceased. The frequency of reciprocal copulation (both members of a pair produced egg masses following copulation) was 95% (35/37 productive matings), higher than previously reported. The duration of egg production ranged from 19 to 197 days (mean ± SE = 110.13 ± 6.3 days) with a sharp drop in production of egg masses and eggs per mass occurring between 15 and 20 weeks postmating, consistent with previous estimates of sperm storage. There was no relationship between mating duration and total egg production (a biomarker of sperm availability) or the duration of egg production (a marker of sperm longevity). Further investigation is needed to directly estimate sperm transfer and tease apart the duration of reciprocal physical contact from gamete and accessory protein transfer.

The gametogenic cycle of an invasive semelparous heterobranch sea slug from northern Patagonia, Argentina, reveals an annual lifespan

This study provides information about the reproductive cycle of the invasive side-gilled sea slug Pleurobranchaea maculata, currently widely distributed along the Argentine coast. The histological analysis of this simultaneous hermaphrodite showed characteristics of a semelparous species with an annual life cycle. The highest spermatogenic and oogenic activity was observed from August to January. Partial evacuations of mature oocytes, measuring over 100 μm in average diameter, occurred continuously during the long spawning season. Oviposition events started in winter and increased in frequency with increasing photoperiod (hours of light) until summer solstices. During February and March, post-reproductive and immature individuals coexisted, while mature individuals were rarely observed. These results represent important information on the reproductive patterns of an invasive species of worldwide ecological and sanitary concern.

Sex-limited experimental evolution drives transcriptomic divergence in a hermaphrodite.

The evolution of gonochorism from hermaphroditism is linked with the formation of sex chromosomes, as well as the evolution of sex-biased and sex-specific gene expression to allow both sexes to reach their fitness optimum. There is evidence that sexual selection drives the evolution of male-biased gene expression in particular. However, previous research in this area in animals comes from either theoretical models or comparative studies of already old sex chromosomes. We therefore investigated changes in gene expression under 3 different selection regimes for the simultaneous hermaphrodite Macrostomum lignano subjected to sex-limited experimental evolution (i.e. selection for fitness via eggs, sperm, or a control regime allowing both). After 21 and 22 generations of selection for male-specific or female-specific fitness, we characterized changes in whole-organism gene expression. We found that female-selected lines had changed the most in their gene expression. Although annotation for this species is limited, gene ontology term and Kyoto Encyclopedia of Genes and Genomes pathway analyses suggest that metabolic changes (e.g. biosynthesis of amino acids and carbon metabolism) are an important adaptive component. As predicted, we found that the expression of genes previously identified as testis-biased candidates tended to be downregulated in the female-selected lines. We did not find any significant expression differences for previously identified candidates of other sex-specific organs, but this may simply reflect that few transcripts have been characterized in this way. In conclusion, our experiment suggests that changes in testis-biased gene expression are important in the early evolution of sex chromosomes and gonochorism.

Xyloplax princealberti (Asteroidea, Echinodermata): A New Species That Is Not Always Associated with Wood Falls

Xyloplax is a genus of three species of sea stars previously found only on sunken wood in the deep ocean. Their circular and petaloid bodies, which lend them their common name “sea daisy”, and their presumed exclusive diet of wood make them an unusual and rare element of deep-sea ecosystems. We describe here the fourth species of Xyloplax from the eastern Pacific Ocean, Xyloplax princealberti n. sp., which ranges from offshore Canada to the Gulf of California (Mexico) and Costa Rica. Though sampled geographically close to another described species of Xyloplax from the northeastern Pacific, X. janetae, this new species is unique morphologically and according to available DNA data. The short abactinal spines are the most obvious feature that distinguishes X. princealberti n. sp. from other Xyloplax. The minimum distance for mitochondrial cytochrome c oxidase subunit I from Xyloplax princealberti n. sp. to the only other available Xyloplax, X. janetae, was 13.5%. We also describe Ridgeia vestimentiferan tubeworm bushes from active hydrothermal vents as a new Xyloplax habitat, the first record of a non-wood substrate, and a new reproductive strategy, simultaneous hermaphroditism, for this genus. We generated the first mitochondrial genome for a member of Xyloplax and analyzed it with other available asteroid data using nucleotide-coding or amino acid (for protein-coding genes) plus nucleotide coding (for rRNA genes). The nucleotide-coding results place Xylopax as part of the clade Velatida, consistent with a previous phylogenomic analysis that included Xyloplax princealberti n. sp. (as Xyloplax sp.), though the placement of Velatida within Asteroidea differed. The amino acid plus nucleotide coding recovered Velatida to be a grade with X. princealberti n. sp. as sister group to all other Asteroidea.

Sexual antagonism in sequential hermaphrodites.

Females and males may have distinct phenotypic optima, but share essentially the same complement of genes, potentially leading to trade-offs between attaining high fitness through female versus male reproductive success. Such sexual antagonism may be particularly acute in hermaphrodites, where both reproductive strategies are housed within a single individual. While previous models have focused on simultaneous hermaphroditism, we lack theory for how sexual antagonism may play out under sequential hermaphroditism, which has the additional complexities of age-structure. Here, we develop a formal theory of sexual antagonism in sequential hermaphrodites. First, we construct a general theoretical overview of the problem, then consider different types of sexually antagonistic and life-history trade-offs, under different modes of genetic inheritance (autosomal or cytoplasmic), and different forms of sequential hermaphroditism (protogynous, protoandrous or bidirectional). Finally, we provide a concrete illustration of these general patterns by developing a two-stage two-sex model, which yields conditions for both invasion of sexually antagonistic alleles and maintenance of sexually antagonistic polymorphisms.

Protandric simultaneous hermaphroditism inSalmoneus carvachoiAnker, 2007 (Decapoda: Alpheidae): a new sexual system in alpheid shrimps

AbstractIn caridean shrimps, sexual systems vary from gonochorism to various forms of hermaphroditism. The shrimp Salmoneus carvachoi has been reported to exhibit both male (appendix masculina) and female (brooding embryos) anatomical characteristics simultaneously. Our aim was to examine the sexual system of S. carvachoi and to test the hypothesis of protandric simultaneous hermaphroditism (PSH) in this species. We analysed internal and external features using microscopy and histology techniques. Our analyses support the hypothesis of PSH in S. carvachoi and enabled the identification of male-phase and hermaphroditic individuals. All individuals exhibit a well-developed appendix masculina on the endopods of the second pleopods; however, small male-phase individuals possess only male gonopores, whereas larger hermaphroditic individuals possess both female and male gonopores. Hermaphrodites exhibit both male and female germinative cells in various stages of development, as well as an androgenic gland. Our study describes a novel sexual system for alpheids and provides a detailed description of anatomical traits in S. carvachoi. Studies that describe sexual systems in Alpheidae may shed light on the evolutionary history of gender expression in carideans and how environmental conditions favour sex allocation in decapods and other invertebrates.

Generic reassignment of Centropristis fuscula Poey, 1861 (Teleostei: Serranidae), with re-description of the species and comments on its geographical range and sexual system.

Centropristes fusculus Poey, 1861 historically has variously and somewhat perplexingly been assigned to Centropristis Cuvier, 1829, Prionodes Jenyns, 1840, and Serranus Cuvier, 1816. Here, we provide evidence from comparisons of morphology, ecology, and sexual systems for its inclusion in Serranus and redescribe the species based on the holotype and 60 specimens from Brazil, the Caribbean, the United States, and Uruguay. Serranus fusculus is a simultaneous hermaphrodite, a sexual system that is relevant to its generic placement. The inclusion of Serranus fusculus in the genus Serranus increases to 33 the number of currently valid Serranus species, of which two are found in the Western Indian Ocean, six in the eastern Pacific and 25 in the Atlantic Ocean (15 restricted to the western Atlantic and 10 to the eastern and Central Atlantic). An identification key to western Atlantic species of the genus is provided.

Age, Growth, and Maturity of Painted Comber Serranus scriba (Serranidae) from the Crimea Region, the Black Sea

The painted comber Serranus scriba, a subtropical marine fish species assigned to the famiy Serranidae in the Black Sea is insufficiently studied. It is a simultaneous hermaphrodite fish. Data on age, growth, and maturity of the painted comber inhabiting the Black sea area around Crimea, including its spatial variation within the entire habitat range are reported. Overall, 537 specimens caught from July to October 2022 are analyzed. The biggest specimen ever caught in the Black Sea with 26.1 cm total length and 265.1 g weight at the age of 15 years was registered. The values for the von Bertalnffy equation parameters were estimated. Thus, asymptotic length, asymptotic weight, and growth constant made up 28.3 cm, 358.6 g, and 0.17 year−1, respectively. The exponent of 3.10 in the length-weight relationship equation (positive allometry) was estimated. Maturity was defined in 50% spesimens at 12.0 ± 0.2 cm total length in the third year of life. It was ascertained that spatial variation in the life history traits for the specimens is weakly expressed. The painted comber inhabiting the Black Sea is slightly different from the representatives of this species found in the Aegean and Adriatic Seas in age, size, and growth. In addition, the biggest and faster-growing specimens are recorded more often under the low-latitude climate conditions, in the water areas off Egypt and the Canary Islands.

Genome-wide identification and expression analysis of Dmrt genes in bivalves

In recent years, some common themes in the development of sex-specific traits in different animal lineages have started to emerge since the discovery of the Dmrt (doublesex-mab3-related transcription factor gene) genes. Bivalves are characterized by a diversity of sexual systems, including simultaneous hermaphroditism, sequential hermaphroditism, and strict gonochorism. However, to date, no research has focused on the genome-wide characterization and analysis of Dmrt genes in bivalves. In this study, the identification and analysis of Dmrt genes in 15 bivalves were performed using bioinformatics methods. A total of 55 Dmrt genes were retrieved in the studied bivalve genomes. The number of Dmrt genes in different species ranged from 3 to 5. The phylogenetic tree showed that Dmrt genes in bivalves can be subdivided into 5 classes: the Dmrt2-like class, Dmrt3-like class, Dmrt4/5-like class, Dsx-like class, and scallop-specific Dmrt class. The Ka/Ks ratios suggested that all Dmrt classes underwent purifying selection pressure. Furthermore, the spatiotemporal expression of Dmrt genes in four bivalve species suggested that different Dmrt genes may have different functions, and scallop-specific Dmrt genes may play a key role in sex determination/differentiation. In general, this study provides a molecular basis for in-depth examination of the functions of Dmrt genes and phylogenomic analyses in bivalves.

K252a inhibition of sperm viability for efficient crossbreeding of hermaphroditic bivalves

Bivalve mollusks are economically important shellfish, representing 56.3% of aquaculture production. Crossbreeding is a popular approach for the genetic improvement of aquaculture species, including bivalves. However, it is difficult for simultaneous hermaphrodites due to the difficulty in collecting unfertilized oocytes. Male infertility or subfertility could be a solution. Considering that protein phosphorylation is critical in spermatogenesis, we investigated the effects of the protein kinase inhibitor K252a on germ cell development, gamete quality and embryonic/larval development of the simultaneously hermaphroditic scallop Argopecten irradians and evaluated its feasibility in crossbreeding. The results showed that 20% K252a injection at the gonad growth stage led to significant decreases in sperm number and progressive motility rate. Abnormal axoneme arrangement in flagella may have caused reduced sperm motility. Normal oocytes fertilized with K252a-treated sperm showed significant decreases in fertilization rate (38.24%), cleavage rate (83.42%) and D-stage survival rate (15.93%), and K252a-treated oocytes did not show obvious defects in early development. Interspecific hybridization using K252a-treated A. irradians fertilized with Argopecten purpuratus sperm resulted in a 3.19-fold increase in the hybrid ratio (67%) over that of the control group (16%). Our study indicated that K252a influenced sperm development without affecting oocytes in A. irradians, indicating that K252a treatment may facilitate the mass production of crossbreeds and hybrids for simultaneous hermaphrodites. The approach reported here will greatly assist in genetic improvement programs for mollusk hermaphrodites.

An Introduction to Diopatra, the Amazing Ecosystem Engineering Polychaete.

The annelid genus Diopatra occurs in all major oceans but is best represented in the shallow depths of warmer waters, where it lives in elaborately decorated tubes. This paper provides an introduction to the animals, discussing their history and diversity. We describe and illustrate its morphology and geographic distribution. While they were thought to be predominantly gonochoristic, recent reproductive studies show that several species are protandric simultaneous hermaphrodites. Development is by broadcast spawning with a brief pelagic stage or direct development in the parental tube or egg mass attached to it. Diopatra is a key ecosystem engineer, altering water flow and deposition and increasing the availability of refugia. We also discuss its harvesting as fishing bait, its role as an alien or introduced species, its capacity to regenerate, its therapeutic potential, and its applications as a bioindicator species for climate change, geographic distribution changes, and dispersal.

A new species of Crasiella (Gastrotricha: Planodasyidae) from Capron Shoal, Florida, USA.

A new gastrotrich species of the genus Crasiella (Macrodasyida: Planodasyidae) is described from Capron Shoal, Florida, USA. The new species is up to 520 μm long and differs from its congeners in the position of adhesive tubes and the structure of its spermatozoa. There are nine TbA that insert ventrally on the head plus an additional pair of TBA that insert medially. Up to 42 TbVL per side. Six pairs of TbP insert on a pair of caudal pedicles. Animals are simultaneous hermaphrodites with an elongated frontal organ and large caudal organ. The spermatozoa have a tripartite acrosome unlike others in the genus that have a four-part acrosome.

Biases in quantitative genetic parameters estimations caused by self-fertilization in the Caribbean pectinid Argopecten nucleus (Mollusca: Bivalvia)

Inbreeding can cause an important bias in the estimates of quantitative genetic parameters, which in turn can affect the estimated potential for a selection response in species that are simultaneous hermaphrodite with partial self-fertilization. In the present study, the biases caused by self-fertilization on heritability (h2) estimates for productive traits were assessed at different ages in the tropical hermaphrodite pectinid Argopecten nucleus. Self-fertilization rates were estimated in both oocytes and adults, as the percentage of zygotes formed from unfertilized oocytes and by paternity analysis using microsatellite genetic markers, respectively. Fifty sexually mature individuals were individually spawned and genotyped using microsatellite markers. The sperm of one individual used as a male was used to fertilize the oocytes of 4 other individuals, generating 10 half-sibling families (HS) and 40 full-siblings families (FS). At the age of 3.5 months, the total weight, and the length, height, and width of the shell of 60 animals per FS family were individually measured. At the age of 9 months, the same measurements were repeated in the same individuals, which were then euthanized to weigh the soft tissues. In addition, the fecundity was estimated in each individual (number of oocytes produced), and a paternity analysis was performed. No significant differences were found in the average inbreeding rates estimated in oocytes and adults. However, no significant correlation was observed in the estimates of family self-fertilization rates when using both methods. The individuals derived from crossbreeding showed higher average values for productive traits than those produced by selfing, although interactions between the genotype and the depth of culture were observed in both groups. The h2 estimates using statistical models that consider self-fertilization in adults (models II and III) were lower than those observed when self-fertilization rates were estimated in oocytes, or not included in the model. However, the genetic correlations between the traits were similar using both methods for estimating self-fertilization rates. The present results suggest that self-fertilization results in inbreeding depression and induces an overestimation of the h2 for productive traits, but it does not affect estimates of genetic correlations or genotype by environment interactions.

Differential masculinization of the chelipeds in two simultaneously hermaphroditic Apseudes tanaidaceans (Crustacea: Malacostraca)

Simultaneous hermaphrodites are uncommon in Malacostraca, having been reported only in Decapoda, Isopoda, and Tanaidacea. Sexual traits not directly related to reproduction, such as masculinization of chelipeds, have received little attention. This study demonstrated that the tanaidacean Apseudes nipponicus Shiino is simultaneously hermaphroditic; and investigated the allometry of chelipeds in two simultaneously hermaphroditic tanaidaceans, A. nipponicus and Apseudes sp. The two species show differential masculinization of the chelipeds. In A. nipponicus, increase in the widths of the chelipedal carpus and chela relative to body size is diphasic, with a higher growth rate in larger individuals. Large individuals also develop ventral spiniform processes on the carpus and a dorsal triangular process on the fixed finger. In Apseudes sp., increase in the widths of the chelipedal carpus and chela relative to body size is monophasic; large individuals fail to develop ventral processes on the carpus but do produce a dorsal process on the fixed finger. The most masculinized state of cheliped development in Apseudes sp. resembles the state in A. nipponicus individuals at an early stage of chelipedal masculinization. Apseudes sp. is smaller in size than A. nipponicus, suggesting that the former might be a progenetic simultaneously hermaphroditic species, achieving earlier maturation as a female by reducing resource allocation to male secondary traits and growth.

A Caenorhabditis elegans Male Pheromone Feminizes Germline Gene Expression in Hermaphrodites and Imposes Life-History Costs.

Sex pheromones not only improve the reproductive success of the recipients, but also impose costs, such as a reduced life span. The underlying mechanisms largely remain to be elucidated. Here, we show that even a brief exposure to physiological amounts of the dominant Caenorhabditis elegans male pheromone, ascr#10, alters the expression of thousands of genes in hermaphrodites. The most dramatic effect on the transcriptome is the upregulation of genes expressed during oogenesis and the downregulation of genes associated with male gametogenesis. This result reveals a way in which social signals help to resolve the inherent conflict between spermatogenesis and oogenesis in a simultaneous hermaphrodite, presumably to optimally align reproductive function with the presence of potential mating partners. We also found that exposure to ascr#10 increased the risk of persistent intestinal infections in hermaphrodites due to pathological pharyngeal hypertrophy. Thus, our study reveals ways in which the male pheromone can not only have beneficial effects on the recipients' reproduction, but also cause harmful consequences that reduce life span.

Sexual Biology and Mating Behaviour in Decapod Crustaceans: A Case Study with Coral Reef Dwelling Caridean Shrimps

Crustaceans have diversified sexual systems, incorporating various reproductive modalities such as gonochorism and a wide variety of hermaphroditism. In particular, the coral reef- dwelling caridean shrimps, living in symbiosis with other marine invertebrates, have developed unusual sexual systems that have given origin to a range of social systems, including the highly advanced eusociality. Protandric hermaphroditism, common among the caridean shrimps, has also reached a unique sexual condition, known as protandric simultaneous hermaphroditism, in the genus, Lysmata. Similarly, mating systems in the caridean shrimps are highly diverse and divergent. In addition, their occurrence in the coral reef shrimps is correlated to their life style adaptations such as their commensal association with other invertebrates. Other ecological factors like the predation risk from outside of the host animals and differences in the host characteristics may also be the driving forces in determining mating associations. Furthermore, the transition from sexual monogamy to social monogamy under conditions of their symbiotic life led to complex community living in several synalpheid shrimps. Understandably, the existence of various sexual and mating systems in these caridean shrimps has a dependence on the eco- social conditions prevalent in the coral reef biota.

Mating motivation: the effect of eliminating the male function on sexual behaviour in a simultaneous hermaphrodite

Mating motivation: the effect of eliminating the male function on sexual behaviour in a simultaneous hermaphrodite