Sex-role Reversed Pipefish Syngnathus Typhle Research Articles

Grandparental immune priming in the pipefish Syngnathus typhle

BackgroundPhenotypic changes in response to environmental influences can persist from one generation into the next. In many systems parental parasite experience influences offspring immune responses, known as transgenerational immune priming (TGIP). TGIP in vertebrates is mainly maternal and short-term, supporting the adaptive immune system of the offspring during its maturation. However, if fathers and offspring have a close physical connection, evolution of additional paternal immune priming can be adaptive. Biparental TGIP may result in maximized immunological protection. Here, we investigate multigenerational biparental TGIP in the sex-role reversed pipefish Syngnathus typhle by exposing grandparents to an immune challenge with heat-killed bacteria and assessing gene expression (44 target genes) of the F2-generation.ResultsGrandparental immune challenge induced gene expression of immune genes in one-week-old grandoffspring. Similarly, genes mediating epigenetic regulation including DNA-methylation and histone modifications were involved in grandparental immune priming. While grand-maternal impact was strong on genes of the complement component system, grand-paternal exposure changed expression patterns of genes mediating innate immune defense.ConclusionIn a system with male pregnancy, grandparents influenced the immune system of their grandoffspring in a sex-specific manner, demonstrating multigenerational biparental TGIP. The involvement of epigenetic effects suggests that TGIP via the paternal line may not be limited to the pipefish system that displays male pregnancy. While the benefits and costs of grandparental TGIP depend on the temporal heterogeneity of environmental conditions, multigenerational TGIP may affect host-parasite coevolution by dampening the amplitude of Red Queen Dynamics.

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.

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.

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.

No terminal investment in pipefish males: only young males exhibit risk-prone courtship behavior

Animals are expected to trade-off current and future reproduction in order to maximize lifetime reproductive success. Old individuals may accept higher risks during courtship and mate choice as their residual reproductive value (RRV) diminishes (the terminal investment hypothesis). Alternatively, young individuals may be forced to take higher risks during courtship to compensate for their lower competitiveness and/or attractiveness (the compensation hypothesis). In this study, we used the sex-role reversed pipefish Syngnathus typhle to test how mate choice and courtship behavior of males with different RRV were affected by an increase in predation risk. Males of different ages were given the opportunity to court and choose between 2 partners. In half of the trials, a predator was present in a separate aquarium. We found no support for the terminal investment hypothesis: no difference in response to the increased predation risk by males of different ages was evident. In agreement with the compensation hypothesis, young males invested more in courtship behavior compared with older males. In addition, in the absence of a predator, we found that a high female activity was important for male mate choice decisions. During increased predation risk, this relationship was, however, reversed and males preferred less active, and thus less conspicuous, partners. This suggests that both female activity and size are important factors for male mating decisions in this species and that these decisions mainly are affected by predation risk and advantages in mate acquisition.

Male pipefish prefer dominant over attractive females

Animals may obtain information guiding their choice between potential partners from observing competitive interactions and displays between them, or from displays directed at the choosing individual. In the sex-role reversed pipefish Syngnathus typhle females display a temporary ornament (a color pattern) to other females as well as to males. We have previously shown that display of female ornaments per se is attractive to males. Here we show that information from competitive displays can override such direct attraction displays as signals in the partner choice process. In a mate choice experiment, an enclosed male could choose between two females. On the first experimental day, females could interact freely, while on the second day they were isolated from each other. When female-female competition was allowed, the ornament display was directed more to the other female than to the male: Time competing, rather than time courting the male, correlated with ornament display duration. However, ornament display under competition and ornament display in the absence of competition did not correlate significantly. In fact, females competing more intensively on day one displayed the ornament less on day two. Furthermore, the ornament display during the first, but not the second, day predicted male mate choice on the second day. Thus, males remembered previous information from competitive displays and used it rather than immediate information from displays in the absence of female-female competition. We suggest that competitive displays more reliably signal female quality as compared to noncompetitive ones, and that males benefit from mating with dominant females.

Male pipefish prefer ornamented females

In the sex-role reversed pipefish Syngnathus typhle females compete for access to males and males are choosy. Females display a temporary ornament, a striped pattern. We show here for the first time in a sex role-reversed species that ornament display predicts how much time a female will devote to competitive behaviours, that males prefer ornamented females over nonornamented ones, and that the ornament is attractive even when female behaviour is held constant. This was demonstrated in an experiment with a male choosing between two females, first with the females separated and then with interactions allowed between the females as well as with the male. Females displaying the ornament for a longer time enjoyed a higher mating success then those displaying the ornament more briefly. Ornament display in the absence of intrasexual competition also predicted the amount of time that females subsequently spent competing. Thus, females initially displaying an attractive trait were also subsequently competing for longer. Furthermore, we manipulated the ornament by painting females and controlled their behaviour by sedating them and moving them in a dance-like fashion by a motor. This experiment showed that males preferred ornamented females, even when female behaviour was standardized. Thus, ornament display accurately predicted the duration of female–female competition and mating success, and was used as a signal by males in their choice of mates.

Female-Female Competition Affects Female Ornamentation in the Sex-Role Reversed Pipefish Syngnathus Typhle

Abstract 1. In the sex role reversed pipefish Syngnathus typhle females compete for males, and males are more choosy than females. Before mating, females display a temporary sexual ornament in the form of a lateral zigzag pattern, which is an amplification of their permanent colour pattern. 2. In experiments males showed no significant preferences for permanently contrast-rich females, nor for females matching closely with the background. 3. Females in physical contact with a male could potentially develop the ornament, but under female-female competition females were more likely to display it than otherwise. 4. The ornament accurately predicted female mating success. More ornamented females displayed more actively towards males and were found closer to males than were non-ornamented females. 5. Females under predation threat were less ornamented than un-threatened females, suggesting a reduced potential for male choosiness under threat. 6. We conclude that the female ornament serves both to attract partners (males) and repel competitors (females).

Ornamentation predicts reproductive success in female pipefish

In the sex-role reversed pipefish Syngnathus typhle females compete for access to males and males are choosy. Females develop a temporary ornament when competing over mates with other females and when performing nuptial dances with males. This ornament is an amplification of the normal striped pattern in these fishes. We here show experimentally that (1) the contrast of this normal pattern forecasts the extent to which the ornament is shown, (2) contrast and ornamentation honestly signal female quality (egg numbers), (3) contrast and ornamentation accurately predict female mating success, (4) contrast is a phenotypically plastic trait specifically exaggerated under situations of female – female competition, and (5) neither contrast nor ornament are energetically expensive to the females (i.e., they are independent of short-term nutritional status). Hence, as predicted in sex-role reversed species, ornament design is constrained by costs to female fecundity: an energetically demanding ornament would impair on a female's ability to produce eggs. The type of ornament described here is the expected one, costly for reasons other than being energetically expensive to produce.

Many Mates Make Male Pipefish Choosy

AbstractIn the sex-role reversed pipefish Syngnathus typhle males search for mates, and prefer to mate with large rather than small females. When mate density was experimentally manipulated, males exerted a mate choice only under high mate density, whereas no mate choice could be demonstrated under low mate density. Hence, when mates are infrequently encountered, males reduce the costs associated with an extended mate search by accepting females that otherwise would have been rejected.