A monogamous pipefish has the same type of ovary as observed in monogamous seahorses

Syngnathid fish (pipefish and seahorses) are unique among teleost fish in that their ovary consists of a rolled sheet with germinal ridge(s) on the dorsal side running along the entire length of the sheet. A distinct difference is seen in the ovarian structure between polygamous Syngnathus pipefish and monogamous seahorses (Hippocampus spp.), the former having one germinal ridge and the latter with two ridges. This study examined the ovarian structure and the mode of egg production in a monogamous pipefish Corythoichthys haematopterus. The ovary of C. haematopterus had two germinal ridges like that observed in monogamous seahorses. There were two distinct groups of follicles in the ovary, one being a cohort of extremely small follicles and the other a cohort of follicles developing and increasing in size with the passage of time. We suggest that the ovarian structure and the mode of egg production in this pipefish are adaptations to monogamy.     

The relationship between female body size and egg size in pipefishes

Comparing five species of pipefish, egg size was significantly larger in species with brood pouches (Syngnathus typhle, Syngnathus acus and Syngnathus rostellatus) than in species without brood pouches (Entelurus aequoreus and Nerophis ophidion). Egg size correlated positively with female body size in species with brood pouches, but was similar across female sizes in the species lacking pouches. These results may reflect differences in offspring competition as a consequence of variable offspring relatedness within a brood, due to the mating systems adopted by the different species and the presence or absence of a brood pouch.     

Straight-nosed pipefish Nerophis ophidion and broad-nosed pipefish Syngnathus typhle avoid eelgrass overgrown with filamentous algae

In a habitat choice experiment straight-nosed pipefish Nerophis ophidion and broad-nosed pipefish Syngnathus typhle avoided eelgrass Zostera marina covered with filamentous algae. Both juveniles as well as brooding adult males of the two species clearly preferred to position themselves in Z. marina without growth of filamentous algae.     

Basic reproductive biology of the barbed pipefish <Emphasis Type="Italic">Urocampus nanus</Emphasis> (Syngnathidae) under laboratory conditions

The mating behaviour, fecundity characteristics and egg production process were investigated in the barbed pipefish Urocampus nanus under aquarium conditions. The mating behaviour consisted of five motor patterns, some of which have been generally reported in other syngnathids. Neither the number nor size of newborns related to the size of parents, although there was a negative correlation between the number and size of newborns. The ovary consisted of two germinal ridges, and mature eggs were produced synchronously with multiple ovulations. This type of egg production has thus far been reported only in a polyandrous and sex-role-reversed pipefish.     

Ovarian structure and mode of egg production in the seaweed pipefish Syngnathus schlegeli (Syngnathidae)

This study investigated ovarian structure and mode of egg production in the seaweed pipefish, Syngnathus schlegeli. The ovary had a rolled sheet-like structure where developing follicles were arranged serially in sequence according to their development, with a single germinal ridge running along the edge of the sheet. Oocytes of various developmental stages were concomitantly present in the ovary, and the number of mature eggs increased continuously over time, indicating that egg production is asynchronous. This would be a physiological basis for multiple spawning within a short time span associated with polygamy in this fish.     

Conventional karyotype, nucleolar organizer regions and genome size in five Mediterranean species of Syngnathidae (Pisces, Syngnathiformes)

Conventional karyotypes, NOR-bearing chromosomes by means of silver impregnation and genome size were investigated in five Mediterranean species in three genera of the Syngnathidae. A karyotype of 48 subtelocentric-acrocentric chromosomes was found in the seahorse Hippocampus hippocampus (FN=48) while a diploid value of 44 occurred in H. guttulatus (2 sm-m+42 a; FN=46) and the pipefish Syngnathus abaster (44 a; FN=44) and S. typhle (44 a; FN=44). The pipefish Nerophis ophidion , possessing a diploid chromosomal set of 58 made up of 50 meta-submetacentric and eight subteloacrocentric elements (FN=108) and a genome size three to four times larger than those known to date, differs cytogenetically from all other Syngnathids studied so far. A single pair of active NOR-bearing chromosomes was found in both species of the genus Hippocampus while in Syngnathus and Nerophis species more than two silver positive chromosomes were found to be involved in nucleolus organization giving rise to NOR-bearing chromosome polymorphism. The possible evolutionary routes of quantitative and qualitative changes in chromosome and DNA are discussed. The resulting phylogenetic scheme is shown to coincide with that constructed from morphological characters.     

Mate quality influences multiple maternity in the sex-role-reversed pipefish Syngnathus typhle

In the pipefish Syngnathus typhle , pregnant males provide all parental care. Females are able to produce more eggs than males can brood, and consequently females compete more intensely for mates than do males, a phenomenon defined as sex-role reversal. As the genetic mating system influences the operation of sexual selection, we investigate variation in one phenotypic component of mate quality, female body size, as a possible proximate influence on mating system variation in S. typhle . Breeding trials were employed, each consisting of a single receptive male with four adult females. In each replicate, a focal male was paired either with a set of small or with a set of large females. Males were allowed to mate freely, and after several weeks of brood development, maternity of the progeny was resolved using three microsatellite loci. Males with access either to small or to large females successfully mated with a mean of 2.1 or 1.3 females, respectively, a significant difference. Results indicate that variation in female size can affect the mating system and thereby influence sexual selection in pipefish. Thus, the high rate of multiple mating by S. typhle males in the wild may be explained in part by the extensive size variation in naturally occurring, sexually mature females.     

Sexual size dimorphism predicts the frequency of multiple mating in the sex-role reversed pipefish Syngnathus typhle

The sex-role reversed pipefish Syngnathus typhle is a member of the Syngnathidae, a family of fishes in which males brood embryos on their body surface. As in most ectotherms, embryonic development is highly temperature dependent in syngnathids and male brooding periods are extended when water temperatures are reduced. The influence of temperature on reproduction is expected to effectively truncate the breeding season and reduce fecundity in cold waters, potentially enhancing the opportunity for both fecundity and sexual selection. We studied spatial variation in the morphology and reproductive biology of S. typhle in five European populations which vary in latitude and water temperature. Microsatellite analyses indicated that the average number of male mates per population ranged between 1.3 and 3.7. The frequency of multiple mating by males was negatively correlated with the degree of sexual size dimorphism in each population, suggesting that disproportionate increases in female fecundity may be able to compensate for increased male brood pouch capacity. Both sexes were larger and males had an increased brood size where water temperatures during the breeding season were lower. Morphological variation among populations may be mediated by differences in fecundity selection associated with different optimal reproductive strategies in cold and warm water environments.     

Sex-specific responses to fecundity selection in the broad-nosed pipefish

Fecundity selection, acting on traits enhancing reproductive output, is an important determinant of organismal body size. Due to a unique mode of reproduction, mating success and fecundity are positively correlated with body size in both sexes of male-pregnant Syngnathus pipefish. As male pipefish brood eggs on their tail and egg production in females occurs in their ovaries (located in the trunk region), fecundity selection is expected to affect both sexes in this species, and is predicted to act differently on body proportions of males and females during their development. Based on this hypothesis, we investigated sexual size dimorphism in body size allometry and vertebral numbers across populations of the widespread European pipefish Syngnathus typhle. Despite the absence of sex-specific differences in overall and region-specific vertebral counts, male and female pipefish differ significantly in the relative lengths of their trunk and tail regions, consistent with region-specific selection pressures in the two sexes. Male pipefish show significant growth allometry, with disproportionate growth in the brooding tail region relative to the trunk, resulting in increasingly skewed region-specific sexual size dimorphism with increasing body size, a pattern consistent across five study populations. Sex-specific differences in patterns of growth in S. typhle support the hypothesis that fecundity selection can contribute to the evolution of sexual size dimorphism.     

Interspecific differences of parental polychlorinated biphenyl exposure on nutrient availability, egg production and brooding in two Syngnathus species

Parental nutrient contribution of two closely related, sympatric pipefish species was investigated following exposure to mid-range environmental concentrations of the polychlorinated biphenyl (PCB) mixture Aroclor 1254 (mean ± s . e . = 52·89 ± 2·12 μg l⁻¹). This study tested the hypothesis that differential nutrient supplementation during development predicts interspecific sensitivity to environmental stressors. Specifically, paternal PCB exposure was predicted to affect Syngnathus fuscus development because embryos depend on paternally derived nutrient sources in the brood pouch. Conversely, changes in Syngnathus floridae egg production were expected following maternal PCB treatment as a nurse-egg system generates the nutrient-rich pouch fluid. Lipid concentrations in adult blood plasma were significantly elevated following Aroclor 1254 treatment in S. floridae gravid females and post-brooding S. fuscus males ( P < 0·001) which suggested mobilization from body tissues in response to metabolic demands. Aroclor 1254 treatment also resulted in decreased protein concentrations in S. fuscus pouch fluid ( P < 0·05). These changes were not translated into significant exposure-related effects in the nutrient reserves of eggs and fry or fry size. Overall S. fuscus demonstrated a general sensitivity to disturbances from laboratory exposure conditions. Whereas a previous investigation of field-collected pipefishes showed comparable interspecific pouch fluid and fry nutrient concentrations and egg size, here, nutrient levels and egg diameter decreased in both laboratory-mated control and PCB-exposed S. fuscus . This study demonstrates the potential physiological effects of PCB exposure on parental nutrient allocation in syngnathids and the general sensitivity of S. fuscus to environmental disturbances.     

The Spawning Behavior of the Pipefish Syngnathus acusimilis

Parental care in representatives of the family Syngnathidae is carried out exclusively by the males and may restrict the reproductive success of the females, resulting in a reversal of their sexual roles. The reversal of the roles of the sexes is specific to polygamous species of the family; it has not been recorded in monogamous species. We describe the spawning behavior of the Primor'e pipefish Syngnathus acusimilis.We show that fish of this species, although polygamous, have no roles reversal between the sexes, and the males are more active during courtship and mate selection.     

Reproductive Biology of Pipefish Syngnathus typhle and S. abaster (Syngnathidae) from Western Mediterranean Sea

Journal of Ichthyology - The reproductive biology of two species of pipefish, Syngnathus typhle and S. abaster, was investigated in western Mediterranean coastal waters, through determination of...     

Sex-role reversal of a monogamous pipefish without higher potential reproductive rate in females

In monogamous animals, males are usually the predominant competitors for mates. However, a strictly monogamous pipefish Corythoichthys haematopterus exceptionally exhibits a reversed sex role. To understand why its sex role is reversed, we measured the adult sex ratio and the potential reproductive rate (PRR), two principal factors influencing the operational sex ratio (OSR), in a natural population of southern Japan. The adult sex ratio was biased towards females throughout the breeding season, but the PRR, which increased with water temperature, did not show sexual difference. We found that an alternative index of the OSR (Sf/Sm: sex ratio of 'time in') calculated from the monthly data was consistently biased towards females. The female-biased OSR associated with sex-role reversal has been reported in some polyandrous or promiscuous pipefish, but factors biasing the OSR differed between these pipefish and C. haematopterus. We concluded that the similar PRR between the sexes in C. haematopterus does not confer reproductive benefit of polygamous mating on either sex, resulting in strict monogamous mating, and its female-biased adult sex ratio promotes female-female competition for a mate, resulting in sex-role reversal.     

Male broad-nosed pipefish Syngnathus typhle do not locate females by smell

Broad-nosed pipefish Syngnathus typhle were used to investigate whether males used scent in their search for mates. When the males in an experiment had access to olfactory cues only, they did not locate females better than they located males. Thus, S. typhle, was less successful in mate search when visual cues were absent.     

Mating systems and sexual selection in male-pregnant pipefishes and seahorses: insights from microsatellite-based studies of maternity

In pipefishes and seahorses (family Syngnathidae), the males provide all postzygotic care of offspring by brooding embryos on their ventral surfaces. In some species, this phenomenon of male "pregnancy" results in a reversal of the usual direction of sexual selection, such that females compete more than males for access to mates, and secondary sexual characteristics evolve in females. Thus the syngnathids can provide critical tests of theories related to the evolution of sex differences and sexual selection. Microsatellite-based studies of the genetic mating systems of several species of pipefishes and seahorses have provided insights into important aspects of the natural history and evolution of these fishes. First, males of species with completely enclosed pouches have complete confidence of paternity, as might be predicted from parental investment theory for species in which males invest so heavily in offspring. Second, a wide range of genetic mating systems have been documented in nature, including genetic monogamy in a seahorse, polygynandry in two species of pipefish, and polyandry in a third pipefish species. The genetic mating systems appear to be causally related to the intensity of sexual selection, with secondary sex characters evolving most often in females of the more polyandrous species. Third, genetic studies of captive-breeding pipefish suggest that the sexual selection gradient (or Bateman gradient) may be a substantially better method for characterizing the mating system than previously available techniques. Finally, these genetic studies of syngnathid mating systems have led to some general insights into the occurrence of clustered mutations at microsatellite loci, the utility of linked loci in studies of parentage, and the use of parentage data for direct estimation of adult population size.     

Genetic evidence for extreme polyandry and extraordinary sex-role reversal in a pipefish.

Due to the phenomenon of male pregnancy, the fish family Syngnathidae (seahorses and pipefishes) has historically been considered an archetypal example of a group in which sexual selection should act more strongly on females than on males. However, more recent work has called into question the idea that all species with male pregnancy are sex-role reversed with respect to the intensity of sexual selection. Furthermore, no studies have formally quantified the opportunity for sexual selection in any natural breeding assemblage of pipefishes or seahorses in order to demonstrate conclusively that sexual selection acts most strongly on females. Here, we use a DNA-based study of parentage in the Gulf pipefish Syngnathus scovelli in order to show that sexual selection indeed acts more strongly on females than on males in this species. Moreover, the Gulf pipefish exhibits classical polyandry with the greatest asymmetry in reproductive roles (as quantified by variances in mating success) between males and females yet documented in any system. Thus, the intensity of sexual selection on females in pipefish rivals that of any other taxon yet studied.     

Ovary of the pipefish,Syngnathus scovelli

Gross dissection, light microscopy, and transmission electron microscopy were used to generate a detailed understanding of the ovarian anatomy of the pipefish, Syngnathus scovelli. The ovary is a cylindrical tube bounded by an outer layer consisting of a smooth muscle wall and an inner layer of luminal epithelium, with follicles sandwiched between the two layers. A remarkable feature of this ovary is a sequential pattern of follicle development. This pattern begins at the germinal ridge with a gradient of follicles of increasing developmental age extending to the mature edge. The germinal ridge is an outpocketed region of the luminal epithelium containing early germinal cells and somatic prefollicular cells. Therefore, the germinal ridge and luminal epithelium share the same ovarian compartment and follicle formation occurs within this compartment. The mature edge is defined as the site of oocyte maturation and ovulation. The outer ovarian wall contains unmyelinated nerve fibers throughout. Longitudinally oriented unmyelinated nerves are also observed near the smooth muscle bundles associated with the mature edge. Oocytes near the mature edge are polarized such that the germinal vesicle (nucleus) is generally oriented toward the luminal epithelium. The sandwichlike organization of the ovary results in follicles that have a shared theca. An extensive lymphatic network is also interspersed among the follicles. Thus, the exceptional features of the pipefish ovary make it particularly well suited for the examination of early events in oogenesis. Specifically, we characterize pipefish folliculogenesis in detail.     

Identification of a uniquely southern African clade of coastal pipefishes Syngnathus spp

The taxonomic status of two southern African coastal pipefish species, Syngnathus temminckii and Syngnathus watermeyeri, was investigated using a combination of morphological and genetic data. Morphological data showed that S. temminckii is distinct from the broadly distributed European pipefish Syngnathus acus, and a molecular phylogeny reconstructed using mitochondrial DNA recovered S. temminckii and S. watermeyeri as sister taxa. The southern African species share an evolutionary origin with north‐eastern Atlantic Ocean and Mediterranean Sea species, including S. acus. These data support the existence of a distinct southern African clade of Syngnathus pipefishes that has diverged in situ to form the two species present in the region today.     

Pipefishes and seahorses: Are they all sex role reversed?

The male pregnancy of pipefishes and seahorses has led to the inference that females compete most intensely for access to mates, because males limit female reproduction. However, recent work has shown that in different species either sex may be the predominant competitor for mates. In this family, there is an apparent association between the mating pattern and the sex roles: polygamous species show reversed sex roles whereas monogamous species exhibit 'conventional' sex roles. These studies emphasize that sex role reversal is not synonymous with male parental care.     

Trophic ecology of two congeneric pipefishes (Syngnathidae) of the lower York River,Virginia

Synopsis The northern pipefish, Syngnathus fuscus, and the dusky pipefish, S. floridae, co-exist in eelgrass beds in the lower York River. To compare the trophic ecology of both pipefishes, gut contents of 3488 northern pipefish, and 1422 dusky pipefish were examined and quantified by dry weight. Samples were taken with a dip net from May through November 1992. Syngnathus fuscus fed mainly on amphipods (Gammarus mucronatus, Amphithoe longimana, and Caprella penantis), and to a lesser degree on copepods, and isopods (Edotea spp. and Erichsonella attenuata). Syngnathus floridae fed mainly on grass shrimps (Palaemonetes pugio, P. vulgaris, and Palaemonetes eggs), and to a lesser degree on copepods, isopods, and mysids (Mysidopsis bigelowi). No seasonal trends were observed in the feeding habits of these pipefishes. Specimens of both species smaller than 100 mm TL fed mainly on copepods. Larger S. fuscus fed on amphipods, while larger S. floridae fed on grass shrimps. Schoener's diet overlap index revealed high consumption of the same prey type by both pipefish species only in July, but only for those specimens smaller than 110 mm TL. Food partitioning between both pipefish was associated with different snout sizes and shapes.