Pipefish Syngnathus Typhle Research Articles

Male mate choice relies on major histocompatibility complex class I in a sex-role-reversed pipefish.

Mate choice for compatible genes is often based on genes of the major histocompatibility complex (MHC). Although MHC-based mate choice is commonly observed in female choice, male mate choice remains elusive. In particular, if males have intense paternal care and are thus the choosing sex, male choice for females with dissimilar MHC can be expected. Here, we investigated whether male mate choice relies on MHC class I genes in the sex-role reversed pipefish Syngnathus typhle. In a mate choice experiment, we determined the relative importance of visual and olfactory cues by manipulating visibility and olfaction. We found that pipefish males chose females that maximize sequence-based amino acid distance between MHC class I genotypes in the offspring when olfactory cues were present. Under visual cues, large females were chosen, but in the absence of visual cues, the choice pattern was reversed. The use of sex-role reversed species thus revealed that sexual selection can lead to the evolution of male mate choice for MHC class I genes.

Candidatus Syngnamydia Venezia, a Novel Member of the Phylum Chlamydiae from the Broad Nosed Pipefish, Syngnathus typhle

Chlamydia are obligate intracellular bacteria and important pathogens of humans and animals. Chlamydia-related bacteria are also major fish pathogens, infecting epithelial cells of the gills and skin to cause the disease epitheliocystis. Given the wide distribution, ancient origins and spectacular diversity of bony fishes, this group offers a rich resource for the identification and isolation of novel Chlamydia. The broad-nosed pipefish (Syngnathus typhle) is a widely distributed and genetically diverse temperate fish species, susceptible to epitheliocystis across much of its range. We describe here a new bacterial species, Candidatus Syngnamydia venezia; epitheliocystis agent of S. typhle and close relative to other chlamydial pathogens which are known to infect diverse hosts ranging from invertebrates to humans.

SEX RATIO AND DENSITY AFFECT SEXUAL SELECTION IN A SEX-ROLE REVERSED FISH

Understanding how demographic processes influence mating systems is important to decode ecological influences on sexual selection in nature. We manipulated sex ratio and density in experimental populations of the sex-role reversed pipefish Syngnathus typhle. We quantified sexual selection using the Bateman gradient (βss'), the opportunity for selection (I), and sexual selection (Is), and the maximum standardized sexual selection differential (smax'). We also measured selection on body length using standardized selection differentials (s') and mating differentials (m'), and tested whether the observed I and Is differ from values obtained by simulating random mating. We found that I, Is, and s'max, but not βss', were higher for females under female than male bias and the opposite for males, but density did not affect these measures. However, higher density decreased sexual selection (m' but not s') on female length, but selection on body length was not affected by sex ratio. Finally, Is but not I was higher than expected from random mating, and only for females under female bias. This study demonstrates that both sex ratio and density affect sexual selection and that disentangling interrelated demographic processes is essential to a more complete understanding of mating behavior and the evolution of mating systems.

Absence of major histocompatibility complex class II mediated immunity in pipefish, Syngnathus typhle : evidence from deep transcriptome sequencing

The major histocompatibility complex (MHC)-mediated adaptive immune system is the hallmark of gnathostome immune defence. Recent work suggests that cod-like fishes (Gadidae) lack important components of the MHC class II mediated immunity. Here, we report a putative independent loss of functionality of this pathway in another species, the pipefish Syngnathus typhle, that belongs to a distantly related fish family (Syngnathidae). In a deep transcriptome sequencing approach comprising several independent normalized and non-normalized expressed sequence tag (EST) libraries with approximately 7.5 × 10(8) reads, sequenced with two next generation platforms (454 and Illumina), we were unable to identify MHC class IIα/β genes as well as genes encoding associated receptors. Along with the recent findings in cod, our results suggest that immune systems of the Euteleosts may be more variable than previously assumed.

The operational sex ratio and density influence spatial relationships between breeding pipefish

The operational sex ratio (ratio of sexually receptive males to females) has been extensively studied in behavioral ecology, whereas other demographic factors such as the effect of density on mating behavior have received less empirical attention. We manipulated mating competition by establishing breeding populations of the sex-role reversed broad-nosed pipefish (Syngnathus typhle) at 2 sex ratios (male biased or female biased) and 2 densities. We used mean crowding (m*) and the index of association (X) to measure spatial distributions within and between the sexes, respectively, and investigated how these measures reflect the predicted strength of mating competition. In general, female m* increased as fewer males were available for mating, which suggests increased intrasexual competition in the most competitive sex. However, male m* also increased as the operational sex ratio became more female biased, suggesting that m* did not reflect mating competition for males. Association between the sexes (X) was higher under male bias than female bias, probably because males were still available for mating under male bias. In addition, X decreased in the female-biased treatment as the operational sex ratio became even more female biased. Higher density increased m* in both sex ratios and sexes, although for both sexes in the female-biased high-density treatment the operational sex ratio did not influence m*, probably because female–female competition inhibits further crowding in this treatment. In this study, we show that the use of m* and X can be a useful tool in behavioral studies but their interpretation requires detailed information about the mating system. Therefore, we recommend caution with their broadscale application.

Altered Oceanic pH Impairs Mating Propensity in a Pipefish

AbstractAnthropogenic disturbance is currently altering the environment of terrestrial as well as aquatic organisms. Those changes affect a variety of animal behaviours, which in turn may cause changes in species interactions, population dynamics and evolutionary processes. In marine ecosystems, nutrient enrichment may elevate pH, while it is reduced by carbon dioxide‐induced ocean acidification. These two processes are not expected to balance one another but rather to affect the environment at different times and scales. We here show experimentally that an increase in water pH has a negative effect on mating propensity in the broad‐nosed pipefish Syngnathus typhle, whereas lowered pH did not elicit the same detrimental effect. This study provides, to our knowledge, the first evidence that mating propensity is impaired by an increase in pH, suggesting that anthropogenic nutrient enrichment in aquatic ecosystems may change the processes of sexual selection and population dynamics solely on the basis of altered water pH.

Salinity change impairs pipefish immune defence

Global change is associated with fast and severe alterations of environmental conditions. Superimposed onto existing salinity variations in a semi-enclosed brackish water body such as the Baltic Sea, a decrease in salinity is predicted due to increased precipitation and freshwater inflow. Moreover, we predict that heavy precipitation events will accentuate salinity fluctuations near shore.Here, we investigated how the immune function of the broad-nosed pipefish (Syngnathus typhle), an ecologically important teleost with sex-role reversal, is influenced by experimentally altered salinities (control: 18 PSU, lowered: 6 PSU, increased: 30 PSU) upon infection with bacteria of the genus Vibrio.Salinity changes resulted in increased activity and proliferation of immune cells. However, upon Vibrio infection, individuals at low salinity were unable to mount specific immune response components, both in terms of monocyte and lymphocyte cell proliferation and immune gene expression compared to pipefish kept at ambient salinities. We interpret this as resource allocation trade-off, implying that resources needed for osmoregulation under salinity stress are lacking for subsequent activation of the immune defence upon infection.Our data suggest that composition of small coastal fish communities may change due to elevated environmental stress levels and the incorporated consequences thereof.

Behavioral adjustments of a pipefish to bacterial Vibrio challenge

Animals can profit from increasing temperatures by prolonged breeding seasons and faster growth rates. However, these fitness benefits are traded off against higher parasite load and increased virulence of temperature-sensitive pathogens. In thermally stratified habitats, behavioral plasticity can allow hosts to choose the optimal temperature to enhance individual fitness and to escape parasite pressure. To test this idea, we performed a temperature choice experiment with the host-parasite system of the sex-role reversed broad-nosed pipefish (Syngnathus typhle) and its bacterial pathogen Vibrio spp. In this species, pregnant males are expected to face a trade-off between shortening their brooding period in warm water and decreasing the effect of the infection in cold water. We found that exposure to Vibrio changed the temperature preference for both pregnant and nonpregnant males, as well as females compared to nonchallenged fish that tended to prefer warm water. This study shows that behavioral plasticity is one option for avoidance of higher bacterial prevalence, as expected due to rising ocean temperatures.

HOSTS ARE AHEAD IN A MARINE HOST-PARASITE COEVOLUTIONARY ARMS RACE: INNATE IMMUNE SYSTEM ADAPTATION IN PIPEFISH SYNGNATHUS TYPHLE AGAINST VIBRIO PHYLOTYPES

Microparasites have a higher evolutionary potential than their hosts due to an increased mutation rate and a shorter generation time that usually results in parasites being locally adapted to their sympatric hosts. This pattern may not apply to generalist pathogens as adaptation to sympatric host genotypes is disadvantageous due to a narrowing of the host range, in particular under strong gene flow among host populations. Under this scenario, we predict that the immune defense of hosts reveals adaptation to locally common pathogen phylotypes. This was tested in four host populations of the pipefish Syngnathus typhle and associated bacteria of the genus Vibrio. We investigated the population divergence among host and bacteria populations and verified that gene flow is higher among host populations than among parasite populations. Next, we experimentally assessed the strength of innate immune defense of pipefish hosts using in vitro assays that measured antimicrobial activity of blood plasma against sympatric and allopatric Vibrio phylotypes. Pipefish plasma displays stronger antimicrobial activity against sympatric Vibrio phylotypes compared to allopatric ones. This suggests that host defense is genetically adapted against local bacteria with a broad and unspecialized host spectrum, a situation that is typical for marine systems with weak host population structure.

Consistent Pattern of Local Adaptation during an Experimental Heat Wave in a Pipefish-Trematode Host-Parasite System

Extreme climate events such as heat waves are expected to increase in frequency under global change. As one indirect effect, they can alter magnitude and direction of species interactions, for example those between hosts and parasites. We simulated a summer heat wave to investigate how a changing environment affects the interaction between the broad-nosed pipefish (Syngnathus typhle) as a host and its digenean trematode parasite (Cryptocotyle lingua). In a fully reciprocal laboratory infection experiment, pipefish from three different coastal locations were exposed to sympatric and allopatric trematode cercariae. In order to examine whether an extreme climatic event disrupts patterns of locally adapted host-parasite combinations we measured the parasite's transmission success as well as the host's adaptive and innate immune defence under control and heat wave conditions. Independent of temperature, sympatric cercariae were always more successful than allopatric ones, indicating that parasites are locally adapted to their hosts. Hosts suffered from heat stress as suggested by fewer cells of the adaptive immune system (lymphocytes) compared to the same groups that were kept at 18°C. However, the proportion of the innate immune cells (monocytes) was higher in the 18°C water. Contrary to our expectations, no interaction between host immune defence, parasite infectivity and temperature stress were found, nor did the pattern of local adaptation change due to increased water temperature. Thus, in this host-parasite interaction, the sympatric parasite keeps ahead of the coevolutionary dynamics across sites, even under increasing temperatures as expected under marine global warming.

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.

Bateman’s principle and immunity in a sex‐role reversed pipefish

In diverse animal species, from insects to mammals, females display a more efficient immune defence than males. Bateman's principle posits that males maximize their fitness by increasing mating frequency whereas females gain fitness benefits by maximizing their lifespan. As a longer lifespan requires a more efficient immune system, these implications of Bateman's principle may explain widespread immune dimorphism among animals. Because in most extant animals, the provisioning of eggs and a higher parental investment are attributes of the female sex, sex-role reversed species provide a unique opportunity to assess whether or not immune dimorphism depends on life history and not on sex per se. In the broad-nosed pipefish Syngnathus typhle, males brood and nourish the eggs in a ventral pouch and thus invest more into reproduction than females. We found males to have a more active immune response both in field data from four populations and also in an experiment under controlled laboratory conditions. This applied to different measures of immunocompetence using innate as well as adaptive immune system traits. We further determined the specificity of immune response initiation after a fully factorial primary and secondary exposure to a common marine pathogen Vibrio spp. Males not only had a more active but also a more specific immune defence than females. Our results thus indeed suggest that the sex that invests more into the offspring has the stronger immune defence.

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.

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.

The ovarian structure and mode of egg production in two polygamous pipefishes: a link to mating pattern

In this study, the ovarian structure and mode of egg production were examined in two pipefishes, the broad-nosed pipefish Syngnathus typhle and the straight-nosed pipefish Nerophis ophidion, which show different types of polygamous mating patterns. Syngnathus typhle showed an ovary with one germinal ridge and asynchronous egg production, corresponding to previous findings in other polygamous Syngnathus pipefishes. In contrast, the ovary of N. ophidion had two germinal ridges and eggs were produced synchronously in groups, similar to what has been observed in monogamous syngnathids. The egg production of N. ophidion, however, is clearly distinguished from that of monogamous syngnathids by the additional egg production after an ovulation. It is suggested that the differences in female mating strategies result from the difference in egg production process and that this is related to the difference in mating pattern between these two polygamous species.

Multiply mated males show higher embryo survival in a paternally caring fish

We explored the effects of multiple mates on male reproductive success in a species with male parental care in which an increase in the number of female mating partners does not increase the number of eggs received. The broad-nosed pipefish (Syngnathus typhle) has a polygynandrous mating system. In this species, the male cares for embryos in a specially developed brood pouch. During brooding, some embryos fail to develop. We experimentally mated males with either one or two females while keeping brood size similar. We found that broods of singly mated males showed significantly lower embryo survival than those of doubly mated males. Furthermore, larger broods showed relatively lower levels of embryo survivorship independent of number of mates. We conclude that embryo survival is affected by postcopulatory processes that appear to result in higher fitness of multiply mated males. We discuss our results in the light of parental care, sibling competition, genetic benefits, and kin selection. Key words: brood reduction, paternal care, polygyny, postcopulatory sexual selection, progeny diversity, Syngnathidae. [Behav Ecol]

Turbidity Hampers Mate Choice in a Pipefish

AbstractEuropean coastal waters have in recent years become more turbid as algal growth has increased, probably due to eutrophication, global warming and changes in fish communities. Turbidity reduces visibility, and such changes may in turn affect animal behaviour as well as evolutionary processes that are dependent on visual stimuli. In this study we experimentally manipulated water visibility and olfactory cues to investigate mate choice using the sex role‐reversed broad‐nosed pipefish Syngnathus typhle as our study organism. We show that males spent significantly longer time assessing females when they had access to full visual cues, compared to when visibility was reduced. Presence or absence of olfactory cues from females did not affect mate choice, suggesting that the possible use of smell could not make up for a reduction in visibility. This implies that mate choice is environmentally dependent and that an increased turbidity may affect processes of sexual selection through an impaired possibility for visually based mate choice.

The description of Gyrodactylus corleonis sp. n. and G. neretum sp. n. (Platyhelminthes: Monogenea) with comments on other gyrodactylids parasitising pipefish (Pisces: Syngnathidae)

The current work describes two new species of Gyrodactylus von Nordmann, 1832 collected from pipefish Syngnathus scovelli (Evermann et Kendall) and Syngnathus typhle L. during two separate gyrodactylosis episodes on fish held in a public aquarium located in northern Italy. The gyrodactylids collected from the skin, fins and gills of pipefish were subjected to a morphological analysis of the attachment hooks and the morphometric data were compared to the four species of Gyrodactylus previously described from syngnathid hosts, namely G. eyipayipi Vaughan, Christison, Hansen et Shinn, 2010, G. pisculentui Williams, Kritsky, Dunnigan, Lash et Klein, 2008, G. shorti Holliman, 1963 and G. syngnathi Appleby, 1996. Principal components analysis (PCA) of the morphological data indicated six clusters; two discrete groups among the specimens taken from the pipefisli held in the Italian aquarium and four further groups representing G. eyipayipi, G. pisculentus, G. shorti and G. syngnathi. Molecular sequences of the ribosomal internal transcribed spacers (ITS1 and ITS2) and the 5.8S gene for the new species considered here were then compared with those available for other species in GenBank. The comparison did not reveal any identical match, supporting the morphological analysis that Gyrodactylus corleonis sp. n. from S. typhle and Gyrodactylus neretum sp. n. from S. scovelli represent distinct species. Both G. corleonis and G. neretum possess robust hamuli, marginal hook blades that curve smoothly from their sickle base to a point beyond the toe and, ventral bars with a broad median portion and a reduced membrane. Gyrodactylus corleonis, however, can be distinguished on the basis of its heart-shaped ventral bar; G. neretum has a 1:2 hamulus point:shaft ratio and a rectangular-shaped ventral bar. A redescription of the haptoral hard parts of the four species previously recorded on pipefish is also presented.

Reproductive compensation in broad-nosed pipefish females

The differential allocation hypothesis assumes that animals should weigh costs and benefits of investing into reproduction with a current mate against the expected quality of future mates, and predicts that they should invest more into reproduction when pairing with a high-quality mate. In the broad-nosed pipefish (Syngnathus typhle), males care for the embryos in a brood pouch and females compete for access to male mating partners. Both sexes prefer mating with large partners. In the present study, we show that the same female provides both large and small mating partners with eggs of similar size, weight and lipid content when mated to two males in succession. Importantly, however, eggs provided to small males (less preferred) had higher egg protein content (11% more) than those provided to large males (preferred). Thus, contrary to the differential allocation hypothesis, eggs did not contain more resources when females mated with a larger male. Instead, the pattern observed in our results is consistent with a compensatory reproductive strategy.

The effect of perceived female parasite load on post-copulatory male choice in a sex-role-reversed pipefish

The last several decades of research in behavioral ecology have resulted in a deeper appreciation of post-mating processes and sexual conflict in sexual selection. One of the most controversial aspects of sexual selection is cryptic mate choice. Here, we take advantage of male pregnancy in a sex-role-reversed pipefish (Syngnathus typhle) to quantify cryptic choice based on perceived parasite load and other sources of variance in female fitness. Studies have shown that S. typhle males preferentially mate with females with lower parasite loads and that a male’s perception of female parasite load can be altered by tattooing females. We manipulated the apparent parasite load of females in controlled mating experiments to test the hypothesis that post-copulatory sexual selection is dependent on a male’s perception of female parasite load in pipefish. Our results provided no evidence for cryptic male choice based on perceived female parasite load. However, we found evidence that eggs from larger females were more likely to result in viable offspring than eggs from smaller females and that the first female to mate with a male transferred more eggs per copulation on average. Overall, our results show that potential for post-copulatory sexual selection does exist in pipefish, but the male’s perception of female parasite load does not play a major role in this process.