Interpopulation morphological variability of the viviparous pipefish Syngnathus acusimilis Günther, 1873 (Teleostei: Syngnathidae)

In viviparous fish, as is illustrated by the example of the pipefish Syngnathus acusimilis (Syngnathidae), unlike fish that spawn their eggs into the environment, there are virtually no differences between populations in meristic characters, which are formed during the embryonic and larval development. The absence of these differences is due to the stability of conditions, specifically temperature, during the egg incubation in the parental organism. The insignificant differences in the external morphology of the pipefish can also be associated with the presence of the bony plates that completely cover the fish body. The peculiarities of the structure and reproductive biology are not conducive to the ecological and geographical intraspecific differentiation of this fish.     

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.     

POLYGYNANDRY IN THE DUSKY PIPEFISH SYNGNATHUS FLORIDAE REVEALED BY MICROSATELLITE DNA MARKERS

In the dusky pipefish Syngnathus floridae, like other species in the family Syngnathidae, ‘pregnant’ males provide all post-zygotic care. Male pregnancy has interesting implications for sexual selection theory and the evolution of mating systems. Here, we employ microsatellite markers to describe the genetic mating system of S. floridae, compare the outcome with a previous report of genetic polyandry for the Gulf pipefish S. scovelli, and consider possible associations between the mating system and degree of sexual dimorphism in these species. Twenty-two pregnant male dusky pipefish from one locale in the northern Gulf of Mexico were analyzed genetically, together with subsamples of 42 embryos from each male's brood pouch. Adult females also were assayed. The genotypes observed in these samples document that cuckoldry by males did not occur; males often receive eggs from multiple females during the course of a pregnancy (six males had one mate each, 13 had two mates, and three had three mates); embryos from different females are segregated spatially within a male's brood pouch; and a female's clutch of eggs often is divided among more than one male. Thus, the genetic mating system of the dusky pipefish is best described as polygynandrous. The genetic results for S. floridae and S. scovelli are consistent with a simple model of sexual selection which predicts that for sex role-reversed organisms, species with greater degrees of sexual dimorphism are more highly polyandrous.     

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.     

The genetic mating system and tests for cuckoldry in a pipefish species in which males fertilize eggs and brood offspring externally

Highly variable microsatellite loci were used to study the mating system of Nerophis ophidion, a species of pipefish in which pregnant males carry embryos on the outside of their body rather than in an enclosed brood pouch. Despite this mode of external fertilization and brooding, otherwise rare in the family Syngnathidae, the genotypes of all embryos proved to be consistent with paternity by the tending male, thus indicating that cuckoldry by sneaker males is rare or nonexistent in this species. N. ophidion is a phylogenetic outlier within the Syngnathidae and its reproductive morphology is thought to be close to the presumed ancestral condition for pipefishes and seahorses. Thus, our genetic results suggest that the evolutionary elaboration of the enclosed brood pouch elsewhere in the family was probably not in response to selection pressures on pregnant males to avoid fertilization thievery. With regard to maternity assignments, our genotypic data are consistent with behavioural observations indicating that females sometimes mate with more than one male during a breeding episode, and that each male carries eggs from a single female. Thus, the polyandrous genetic mating system in this species parallels the social mating system, and both are consistent with a more intense sexual selection operating on females, and the elaboration of secondary sexual characters in that gender.     

Microsatellite analysis of maternity and the mating system in the Gulf pipefish Syngnathus scovelli, a species with male pregnancy and sex-role reversal

Highly variable microsatellite loci were employed to study the mating system of the sexually dimorphic Gulf pipefish Syngnathus scovelli . In this species, like others in the family Syngnathidae, 'pregnant' males provide all parental care. Gulf pipefish were collected from one locale in the northern Gulf of Mexico, and internally carried broods of 40 pregnant males were analysed genetically. By comparing multilocus microsatellite fingerprints for the inferred mothers against expected genotypic distributions from the population sample, it was determined that: (i) only one male had received eggs from more than a single female; and (ii) on two separate occasions, two different males had received eggs from the same female. Given the high power to detect multiple matings by males, the first finding indicates that only rarely are individual males impregnated by multiple females during the course of a pregnancy. Conversely, given the lower power to detect multiple matings by females due to sampling constraints, the second finding suggests a high frequency of multiple successful matings by females. Thus, this population of Gulf pipefish displays a polyandrous genetic mating system. The relevance of these genetic findings is discussed with regard to the evolution of secondary sex traits in this species, and in other syngnathids.     

The dynamics of male brooding,mating patterns,and sex roles in pipefishes and seahorses (family Syngnathidae)

Modern theory predicts that relative parental investment of the sexes in their young is a key factor responsible for sexual selection. Seahorses and pipefishes (family Syngnathidae) are extraordinary among fishes in their remarkable adaptations for paternal care and frequent occurrences of sex-role reversals (i.e., female-female competition for mates), offering exceptional opportunities to test predictions of sexual selection theory. During mating, the female transfers eggs into or onto specialized egg-brooding structures that are located on either the male's abdomen or its tail, where they are osmoregulated, aerated, and nourished by specially adapted structures. All syngnathid males exhibit this form of parental care but the brooding structures vary, ranging from the simple ventral gluing areas of some pipefishes to the completely enclosed pouches found in seahorses. We present a molecular phylogeny that indicates that the diversification of pouch types is positively correlated with the major evolutionary radiation of the group, suggesting that this extreme development and diversification of paternal care may have been an important evolutionary innovation of the Syngnathidae. Based on recent studies that show that the complexity of brooding structures reflects the degree of paternal investment in several syngnathid species, we predicted sex-role reversals to be more common among species with more complex brooding structures. In contrast to this prediction, however, both parsimony- and likelihood-based reconstructions of the evolution of sex-role reversal in pipefishes and seahorses suggest multiple shifts in sex roles in the group, independent from the degree of brood pouch development. At the same time, our data demonstrate that sex-role reversal is positively associated with polygamous mating patterns, whereas most nonreversed species mate monogamously, suggesting that selection for polygamy or monogamy in pipefishes and seahorses may strongly influence sex roles in the wild.     

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.     

Morphological variation in head shape of pipefishes and seahorses in relation to snout length and developmental growth

The feeding apparatus of Syngnathidae, with its elongate tubular snout and tiny, toothless jaws, is highly specialized for performing fast and powerful pivot feeding. In addition, the prolonged syngnathid parental care probably enables the juveniles to be provided with a feeding apparatus that resembles the one in adults, both in morphology and function. In this study, a landmark‐based geometric morphometric analysis was carried out on the head of syngnathid representatives in order to (1) examine to what degree pipefish shape variation is different from that of seahorses; (2) determine whether the high level of specialization reduces the amount of intraspecific morphological variation found within the family; and (3) elucidate whether or not important shape changes occur in the seahorse head during postrelease ontogeny. We found that (1) there is a significant shape difference between head shape of pipefish and seahorse: the main differences concern snout length and height, position and orientation of the pectoral fin base, and height of the head and opercular bone. We hypothesize that this might be related to different prey capture kinematics (long snout with little head rotation versus short snout with large head rotation) and to different body postures (in line with the head versus vertical with a tilted head) in pipefishes and seahorses; (2) both pipefishes and seahorses showed an inverse relation between relative snout length and intraspecific variation and although pipefishes show a large diversity in relative snout elongation, they are more constrained in terms of head shape; and (3) the head of juvenile Hippocampus reidi specimens still undergoes gradual shape changes after being expelled from the brood pouch. Ontogenetic changes include lowering of the snout and head but also differences in orientation of the preopercular bone and lowering of the snout tip. J. Morphol. 2011. © 2011 Wiley‐Liss, Inc.     

Validation of otolith daily increment formation for two temperate syngnathid fishes: the pipefishes Stigmatopora argus and Stigmatopora nigra

Otoliths were used for the first time to successfully validate the age of members of the family Syngnathidae: the spotted pipefish Stigmatopora argus and the wide-bodied pipefish Stigmatopora nigra. Otolith increments were deposited daily in (1) known-age juveniles ranging in age from 0 to 31 days and (2) adults that had been stained with alizarin complexone, and a hatch mark was found on all otoliths which represented day 0. Otolith increment validation will allow development of growth models for S. argus and S. nigra, essential to understanding and managing these exclusive seagrass species.     

Osmoregulatory role of the brood pouch in the euryhaline Gulf pipefish, Syngnathus scovelli

Many species of pipefish exhibit a reversal of parental roles, in which females insert eggs into the brood pouch of the male where they are incubated until the end of embryonic development. While the significance of the male brood pouch has been examined for over a century, the role of the pouch is still unclear. One possible function is to aid in osmoregulation by buffering embryos from the external environment. To investigate this role, the euryhaline Gulf pipefish, Syngnathus scovelli, was collected and maintained in either a low salinity or a saltwater environment. Changes in plasma and pouch fluid osmolality and morphological changes of the pouch were examined. Brood pouch fluid was similar to male plasma during the early and late stages of the brooding period for low salinity males, but was significantly hyperosmotic during the middle of the brooding period. In saltwater males, brood pouch fluid was similar to plasma during early brooding, but became hyperosmotic as brood time progressed. The brood pouch epithelium of both low salinity and saltwater males contained mitochondria-rich cells. In early brooding saltwater males these cells contained an apical opening into the pouch lumen. Osmotic and morphological differences observed suggest that the brood pouch plays an active role in regulating osmotic concentration of the pouch fluid. Additionally, pouch fluid concentration may be regulated more during early stages of embryonic development.     

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.     

Reproduction and spawning behavior of the climbing perch Anabas testudineus (Perciformes, Anabantidae) in an aquarium

Results of study of the spawning and reproductive behavior of the climbing perch Anabas testudineus in an aquarium are presented. Main specific features of reproduction of this species are revealed. In the performed experiments, climbing perches did not build a nest, did not prepare a spawning substrate, and did not show any forms of parental care. The pre-spawning and spawning behavior of the climbing perch is described, and fecundity and gonadosomatic index are determined. It is shown that intermittent spawning is typical of these fish. Mating system of the climbing perch is either polygamy or promiscuity. Sexual dimorphism in the climbing perch was not found. The eggs of the climbing perch have positive buoyancy and belong to the really pelagic type, which is rare for freshwater fish. Infanticide is a common phenomenon for the climbing perch. Breeding of the given species under aquarium conditions can be exercised without artificial hormonal stimulation, at different sex ratio, and under conditions of stocking density considerably exceeding standard aquacultural recommendations. The main specific features of reproduction of the climbing perch are discussed in relation to evolution of parental care in labyrinth fishes.     

Fecundity selection predicts Bergmann's rule in syngnathid fishes

The study of latitudinal increases in organismal body size (Bergmann's rule) predates even Darwin's evolutionary theory. While research has long concentrated on identifying general evolutionary explanations for this phenomenon, recent work suggests that different factors operating on local evolutionary timescales may be the cause of this widespread trend. Bergmann's rule explains body size variation in a diversity of warm-blooded organisms and there is increasing evidence that Bergmann's rule is also widespread in ectotherms. Bergmann's rule acts differentially in species of the Syngnathidae, a family of teleost fishes noted for extreme adaptations for male parental care. While variation in body size of polygamous Syngnathus pipefish is consistent with Bergmann's rule, body size is uncorrelated with latitude in monogamous Hippocampus seahorses. A study of populations of Syngnathus leptorhynchus along a natural latitudinal and thermal gradient indicates that increases in body size with latitude maintain the potential reproductive rate of males despite significant decreases in ambient temperatures. Polygyny is necessary in order to maximize male reproductive success in S. leptorhynchus , suggesting a possible a link between fecundity selection and Bergmann's rule in this species.     

PATTERNS OF PARENTAL CARE AND PARENTAL INVESTMENT IN MARSUPIALS

I. Information on growth, development and care of young has been assembled for 62 species of marsupial. 2. During gestation, development of the marsupial embryo proceeds only so far as to allow the neonate to make its way from the urogenital opening to the mammary area on the abdomen of the female where it attaches to a teat. Specific structural adaptations keep the neonate firmly attached to the teat for at least the first month after birth. 3. Six types of pouch are distinguished ranging from lateral folds of skin, which do not cover the mammary area or enclose the developing young, to a fold of skin that covers the mammary area and forms a deep pouch, completely enclosing the developing young. 4. Although the young is very small at birth and birth is rapid, specific changes in the behaviour of females occur around the time of birth, and a specific birth position is adopted. 5. The time at which marsupial young leave the pouch cannot be equated with birth in eutherians, because of the considerable variations in the type of pouch and in patterns of parental care. From a consideration of the functional development of the young in the pouch, it is suggested that the nearest equivalent to eutherian birth is the time at which the marsupial young achieves homeostasis, when it is well furred and endothermic. 6. Maternal behaviour is influenced by the type of pouch. In all species, the mother keeps the young and the pouch clean by licking, especially when the young are wholly within the pouch or attached to the abdomen. In species with reduced pouches where young are left in a nest at an early stage of development, maternal behaviour includes nest building, defence, and retrieving and carrying the young. These functions are performed by the pouch itself in species with large deep pouches in which the young is carried for a much larger part of its development, and other specific maternal behaviours are infrequent. 7. The patterns of parental care are reviewed over all families of marsupial. Not all members of a family have the same pattern of parental care, which appears to be influenced by many factors including body size, type of pouch, diet, litter size and other aspects of life history strategy. 8. Three patterns of parental care are distinguished: (A) As soon as young begin to release the teat they are no longer carried by the mother, and are left in a nest when still barely furred, ectothermic and before the eyes open. This pattern is found in species with large litter size and a pouch reduced or absent, e.g. some Dasyuridae and some Didelphidae. (B) Young remain in the pouch after they begin to release the teat but are left in a nest, at a later stage of development than in A, when well furred, endothermic and with eyes open. After first pouch exit, there is generally a period when young return to the pouch from time to time. This pattern is found in species with well developed pouches and litters of I or > 1 e.g. Peramelidae, some Didelphidae. (C) Young remain in the pouch after they begin to release the teat. At first pouch exit, the young is well furred and endothermic, and leaves the pouch only for brief periods, gradually spending more time out until permanent pouch exit. It is not usually left in a nest. This pattern is found in species with well developed pouches and litters of one, e.g. Macropodidae. 9. Pattern A is seen particularly in the smaller species in any family, where large litter size means that by the time young release the teat, the litter is about 50% of maternal body weight and a considerable burden. In such species, young are left in a nest as soon as possible. In larger species with patterns B or C, litter size is smaller, and by the time they are no longer carried by the female, the litter is still only 20% of maternal weight. 10. Whatever the pattern of parental care, mortality from birth to permanent pouch exit is not unusually high in marsupials in comparison with eutherians. 11. I suggest that the presence of the pouch and the associated patterns of parental care are important determinants of social organization in marsupials. For much of the period of dependence, the young is small, attached to a teat or in a pouch. The male can make little contribution to parental care, and there is little room for improvement in the care of young in complex social groups. In most species, the female on her own is sufficient caretaker. The male is most likely to increase his own biological fitness by going off to mate again and leaving the female to raise his offspring. 12. Patterns of energy expenditure on offspring by female marsupials were assessed throughout the development of young. Investment before birth was assessed by weight of the neonate, during development by growth rate and the time for which the young was carried (pouch life), and total investment by weight of young at weaning and time from birth to weaning. Regression of measures of investment against maternal body weight allowed comparison of investment in animals of different size. 13. Investment in young before birth is very small. Neonatal marsupials range in size from 0·01 to 1 g, and the largest is less than 0·2 % of the size of the mother. Larger mothers produce larger young which are smaller relative to the mother than are the young of smaller species. Individual young in the family Dasyuridae are particularly small. 14. Growth rates in g/d were calculated over the period from permanent pouch exit to weaning. There is a very close correlation between growth rate and maternal body weight - that of litters increases as the 0·78 power of body weight. During this period the growth rate of individuals is comparable with that of eutherian young during lactation, and in litters it is higher still, suggesting that the difference in patterns of growth are not due to the lower metabolic rate of marsupials. As in eutherians there is considerable individual variation in growth rate; it is very high in litters of small dasyurids, which have individual rates comparable to those of larger species. Young of the family Peramelidae grow and develop rapidly; those of the arboreal folivore Phascolarctos do both slowly. I 5. Pouch life, the period for which the young is carried by the mother, increases with body size; as expected, species with pattern A parental care have shorter pouch lives than species of the same size with patterns B or C, reflecting the early stage of development at which young are left in the nest in pattern A. 16. Time from birth to weaning is also longer in larger species. There is a close relationship of age at weaning with maternal weight, with some significant exceptions. For their size, the family Peramelidae have a very short time from birth to weaning, and the time from pouch exit to weaning is particularly short. Many arboreal species have longer periods of dependence than expected from their size. 17. The weight at weaning of individual young is closely related to MBW^0·71, but the weight of one young relative to maternal body weight shows no trend with size, and ranges from 25–61 %, with a mean of 42 %. 18. Parental Investment, as measured by the function Wt. of litter at weaning × 100/MBW, decreases with increasing size of mother as MBW^0·28. The highest levels of investment are found in very small species. In many small species of the family Dasyuridae, a litter at weaning is > 300% MBW. By contrast, investment in the family Peramelidae is low - at weaning a litter of three is about 50% MBW, comparable with investment in a single young of the family Macropodidae. 19. The evolution of patterns of parental care and investment appears to follow three main lines: (1) Species with large litter size, high levels of investment in litters and in individual young. Investment is directed to growth and not to carrying the young in the pouch, since young are left in a nest at an early stage. Typical of this group is the family Dasyuridae, in which many species make few reproductive attempts per year. (2) Species with litters of more than one, low levels of investment in litters and in individuals, but rapid growth and development of young. Because of the small relative size of young they are carried in the pouch for a large part of the period from birth to weaning. This pattern is shown by the family Peramelidae, and seen as an adaptation to rapid and repeated reproduction in an environment with an extended favourable season. (3) Species with small litter size, lower total investment, but investment in individual young is not low, and investment in carrying young to an advanced stage of development is high. Patterns of this type are found in the Diprotodonta, with extreme development in the Macropodidae. 20. Many of the measures of investment have been expressed as a power function of maternal body weight. The exponents of body weight in these functions are such as to suggest that an important underlying variable is metabolic rate. 21. It has been suggested elsewhere that the marsupial mode of reproduction evolved as an adaptation to environmental uncertainty, in that it allows a reproductive attempt to be abandoned at any time much more readily than in eutherians, thereby increasing the likelihood that a female will survive to reproduce again. I consider this suggestion in the light of patterns of parental investment. For small, short-lived species, any reproductive attempt represents a substantial part of its lifetime reproductive output. Investment in any one reproductive attempt is high, and the cost of replacing an abandoned attempt is so high that it seems unlikely that the desertion of offspring would be an important reproductive strategy in small ancestral marsupials, although it may be an important response to environmental uncertainty in certain large modern macropodids.     

Monogamy and sex role reversal in the pipefish Corythoichthys haematopterus

We observed the mating pattern and social behaviour of the pipefish Corythoichthys haematopterus in temperate waters of Japan during three successive breeding seasons. Males cared for a clutch in their brood pouch for 9-19 days until hatching and had several broods in the season with nonbrooding intervals of only 1 or 2 days. The population sex ratio was female biased and some females were always excluded from reproduction. Although males were sometimes courted by unmated females together with their regular partners, they always mated with the latter. The pair bond was maintained until the next season if both members survived. When males lost their partners, they remated with neighbouring unmated females within a few days. In contrast, widowed females remained unmated for a long time. Females had larger home ranges and were more active in courtship displays than males. This pipefish provides the first example of sex role reversal among monogamous syngnathid fish. We suggest that mate guarding by females is a primary proximate factor for maintenance of monogamy in this fish. Copyright 2001 The Association for the Study of Animal Behaviour.     

Brooding season, sex ratio, and brood pouch development in the seaweed pipefish, Syngnathus schlegeli, in Otsuchi Bay, Japan

Males of the seaweed pipefish, Syngnathus schlegeli, take care of their eggs in the brood pouch. These pipefish were periodically collected from the shallow seagrass beds in Otsuchi Bay on the Pacific coast of northern Honshu, Japan, from spring to autumn to investigate the basic reproductive ecology. Appearance of the pipefish in the coastal seagrass beds coincided with the initiation of reproduction. The reproductive season was from May to at least October, with its peak in July. A rearing experiment revealed that the brooding period of the male had a negative correlation with water temperature, and it was estimated to last about 1 month in the bay. Almost all males were brooding during the peak of the reproductive season. Although, the brood pouch of most males was either full or devoid of eggs, 6.2% of the males had a partially filled (20%–90%) brood pouch, and multiple clutches were identified in the brood pouch of some males, indicating that the mating system of the pipefish is polygamous, perhaps polygynous. Sex ratio fluctuated among months, and the overall sex ratio tended to be biased to male. Body size of males with an immature brood pouch had a wide range, from 133 to 215 mm standard length (SL). The smallest brooding male was 134 mm SL. Mean SL of brooding males was significantly larger than that of nonbrooding mature males. The number of males with an immature brood pouch was greater at the beginning than later in the reproductive season. The results seem to collectively indicate that the occurrence of a larger proportion of immature males at the onset of the reproductive season may be ascribed to both new recruitment and larger body size at maturation, resulting from the males trading the reproductive effort to somatic growth, perhaps to increase future reproductive success. Received: April 4, 2000 / Revised: September 21, 2000 / Accepted: January 16, 2001     

The Effects of Food Limitation on Life History Tradeoffs in Pregnant Male Gulf Pipefish

Syngnathid fishes (pipefishes, seahorses and seadragons) are characterized by a unique mode of paternal care in which embryos develop on or in the male’s body, often within a structure known as a brood pouch. Evidence suggests that this pouch plays a role in mediating postcopulatory sexual selection and that males have some control over the events occurring within the pouch during the pregnancy. These observations lead to the prediction that males should invest differently in broods depending on the availability of food. Here, we use the Gulf pipefish to test this prediction by monitoring growth rate and offspring survivorship during the pregnancies of males under low- or high-food conditions. Our results show that pregnant males grow less rapidly on average than non-pregnant males, and pregnant males under low-food conditions grow less than pregnant males under high-food conditions. Offspring survivorship, on the other hand, does not differ between food treatments, suggesting that male Gulf pipefish sacrifice investment in somatic growth, and thus indirectly sacrifice future reproduction, in favor of current reproduction. However, a positive relationship between number of failed eggs and male growth rate in our low-food treatments suggests that undeveloped eggs reduce the pregnancy’s overall cost to the male compared to broods containing only viable offspring.     

Bacteria‐type‐specific biparental immune priming in the pipefish Syngnathus typhle

The transfer of acquired and specific immunity against previously encountered bacteria from mothers to offspring boosts the immune response of the next generation and supports the development of a successful pathogen defense. While most studies claim that the transfer of immunity is a maternal trait, in the sex‐role‐reversed pipefish Syngnathus typhle, fathers nurse the embryos over a placenta‐like structure, which opens the door for additional paternal immune priming. We examined the potential and persistence of bacteria‐type‐specific parental immune priming in the pipefish S. typhle over maturation time using a fully reciprocal design with two different bacteria species (Vibrio spp. and Tenacibaculum maritimum). Our results suggest that S. typhle is able to specifically prime the next generation against prevalent local bacteria and to a limited extent even also against newly introduced bacteria species. Long‐term protection was thereby maintained only against prevailing Vibrio bacteria. Maternal and paternal transgenerational immune priming can complement each other, as they affect different pathways of the offspring immune system and come with distinct degree of specificity. The differential regulation of DNA‐methylation genes upon parental bacteria exposure in premature pipefish offspring indicates that epigenetic regulation processes are involved in transferring immune‐related information across generations. The identified trade‐offs between immune priming and reproduction determine TGIP as a costly trait, which might constrain the evolution of long‐lasting TGIP, if parental and offspring generations do not share the same parasite assembly.     

Male pregnancy in seahorses and pipefishes (family Syngnathidae): rapid diversification of paternal brood pouch morphology inferred from a molecular phylogeny

In contrast to the majority of vertebrate species, primary male parental care is common in fishes and encompasses a remarkable diversity of adaptations. Seahorses and pipefishes (Family Syngnathidae) exhibit some of the most specialized forms of paternal care in animals and so are ideally suited to the study of the evolution of male parental care. During mating, female syngnathids transfer eggs to specialized morphological structures that are located on either the abdomen or tail of the male. The male provides all postfertilization parental care and has morphological and physiological adaptations to osmoregulate, aerate, and even nourish the developing embryos. While all syngnathid species are adapted for paternal care, the brooding structure with which this is accomplished varies between species, from simple ventral gluing areas to much more complex structures such as the completely enclosed pouches of the seahorses. Our combined cytochrome b-, 12S rDNA-, and 16S rDNA-based molecular phylogeny of syngnathid fishes demonstrates that rapid diversification of male brooding structures has been associated with the major evolutionary radiation of the group, suggesting that development and diversification of structures involved in paternal care may have been key evolutionary innovations of the Syngnathidae. Molecular analyses also highlight geographical centers of biodiversity and suggest interoceanic migration of Syngnathus pipefishes from their center of origin in the Pacific.