Gunilla Rosenqvist

Mate choice, fecundity and sexual dimorphism in two pipefish species (Syngnathidae)

SummaryIn order to understand the causes of sexual dimorphism, mate choice and size-related fecundity were studied in two pipefish species, Syngnathus typhle and Nerophis ophidion. Sexual dimorphism is more pronounced in N. ophidion; females are larger, have sexual colourings, and are more active during courtship. In S. typhle the sexes are alike in all these respects. Males brood their offspring in both species. In N. ophidion fecundity was positively correlated with both body size and the amount of sexual colouring in females. In males no correlation between body size and fecundity, or between body size and embryo size existed. Predictably, in mate choice experiments with equal-sized females, males chose females with more extensive sexual colourings. We explain sexual dimorphism in this species as a consequence of both natural selection (fecundity increases with size in females but not in males) and sexual selection (males prefer larger females). We argue that sexual size dimorphism did not evolve by selection minimizing overlap in food niches between the sexes, because food production is high in the Zostera beds where the fishes live, and no size dimorphism was found in the sympatrically occurring S. typhle. Furthermore, in N. ophidion dimorphism is not greater in a particular mouth character than in overall body size. In S. typhle egg size and the average number of eggs transferred per spawning were positively correlated with female body size. Apparently more energy per offspring was provided by larger males than by smaller males, and larger males also carried more offspring. As predicted, large mates were preferred by both sexes in mate choice experiments. This is explicable in terms of both natural selection (fecundity increases with size in both sexes) and sexual selection (both sexes prefer large mates). As a consequence of selection acting in the same direction in both sexes, sexual dimorphism is absent in S. typhle.

Sex Role Reversal in Pipefish

Publisher Summary The chapter presents the problem in two sex role-reversed pipefish species. The chapter discusses why potential reproductive rates differ and the consequences of this “reversed” mating competition on sexually selected traits in females. Potential reproductive rates—that is, how fast males and females can potentially remate, given that partner availability is not limiting, and operational sex ratios, that is, the proportion of males and females willing to mate are instrumental in understanding this pattern. In two sex role-reversed pipefish species, Syngnathus typhle and Nerophis ophidion, males devoted more time, but not more energy, than females to offspring production. The chapter outlines the costs and benefits of these sexually selected traits and mating preferences to allow for a better understanding of sexual selection processes in sex role-reversed species and understands the very same processes in species with conventional sex roles. The chapter explains that sex role reversal and female ornamentation seem intimately linked with paternal care and how that paternal care may have evolved in syngnathids and how sex role reversal in pipefish is ultimately a consequence of an extreme level of paternal care in combination with a polygamous mating pattern are discussed.

The Bateman gradient and the cause of sexual selection in a sex–role–reversed pipefish

As a conspicuous evolutionary mechanism, sexual selection has received much attention from theorists and empiricists. Although the importance of the mating system to sexual selection has long been appreciated, the precise relationship remains obscure. In a classic experimental study based on parentage assessment using visible genetic markers, more than 50 years ago A. J. Bateman proposed that the cause of sexual selection in Drosophila is ‘the stronger correlation, in males (relative to females), between number of mates and fertility (number of progeny)’. Half a century later, molecular genetic techniques for assigning parentage now permit mirror–image experimental tests of the ‘Bateman gradient’ using sex–role–reversed species. Here we show that, in the male–pregnant pipefish Syngnathus typhle, females exhibit a stronger positive association between number of mates and fertility than do males and that this relationship responds in the predicted fashion to changes in the adult sex ratio. These findings give empirical support to the idea that the relationship between mating success and number of progeny, as characterized by the Bateman gradient, is a central feature of the genetic mating system affecting the strength and direction of sexual selection.

Male mate choice and female-female competition for mates in the pipefish Nerophis ophidion

Abstract Male mate choice and female-female competition for access to mates were studied in the pipefish Nerophis ophidion , with the aim of evaluating the function and importance of female size and ornamental skin folds. Nerophis ophidion is sex role-reversed in the sense that paternal care limits female reproductive success. Furthermore, females are larger, possess a sexual coloration, and develop an ornamental skin fold during the spawning season. Females are also more active than males during courtship. In mate-choice experiments males actively preferred both larger females and females with larger skin folds. When several females were kept together, only one female in each group developed a large skin fold. Females interacting only with males invariably developed skin folds whereas isolated females did not. The skin fold affects choice of females by males, and since females are socially stimulated to develop their skin fold, interaction with conspecifics indirectly affects male mate choice. Female-female interactions may suppress the development of the skin fold. Hence, both active male mate choice based upon female secondary sexual characters and female-female interactions determine the non-random mating pattern observed.

The genetic mating system of a sex-role-reversed pipefish (Syngnathus typhle): a molecular inquiry

Abstract In the pipefish Syngnathus typhle as in other species of Syngnathidae, developing embryos are reared on the males ventral surface. Although much laboratory research has been directed toward understanding sexual selection in this sex-role-reversed species, few studies have addressed the mating behavior of S. typhle in the wild, and none has capitalized upon the power of molecular genetic assays. Here we present the first direct assessment of the genetic mating system of S. typhle in nature. Novel microsatellite loci were cloned and characterized from this species, and employed to assay entire broods from 30 pregnant, field-captured males. Genetic analysis of 1340 embryos revealed that 1–6 females (mean = 3.1) contributed to each brooded clutch, the highest rate of multiple maternity yet documented in any pipefish. Evidence of multiple mating by females was also detected. Thus, this population of S. typhle displays a polygynandrous mating system, a finding consistent with previous field and laboratory observations. Our results, considered together with similar studies of other syngnathid species, provide preliminary support for the hypothesis that the genetic mating system is related to the evolution of sexual dimorphism in the fish family Syngnathidae.

Selective males and ardent females in pipefishes

SummaryIn the pipefishes Syngnathus typhle and Nerophis ophidion, males have been shown to limit female reproductive rate, and females to compete for access to males. Hence, these species fit the criteria for sex-role reversal. Males brood the eggs and provide the offspring with nutrients, oxygen and an osmoregulated environment. Moreover, in S. typhle both sexes prefer a larger mate when given a choice. Sexual selection theory predicts that males should be more “choosy” than females, and that was experimentally demonstrated in this study. We predicted that S. typhle males should be less eager to copulate than S. typhle females with an unattractive (i.e. small) mate. We measured eagerness as the time from the start of the experiment until copulation occurred. Males with unattractive partners took significantly longer to copulate than females with unattractive partners. Moreover, females invariably initiated the courtship dance, and resumed it quicker after copulation than did the males, again suggesting “reproductive hesitation” in males. Neither male nor female size per se was correlated with time until copulation. In N. ophidion, where we have previously shown that males prefer larger to smaller females, we found that females did not select males with regard to size. Our results are consistent both with earlier findings (males limit female reproduction and females compete for males) and with operational sex ratios in nature: in seven annual field samples in June, the numbers of S. typhle females with ripe eggs always significantly exceeded numbers of receptive males. Hence, the potential cost of being choosy in terms of lost matings is much higher in females than in males. In conclusion, S. typhle females were somewhat choosy, but less so than males, whereas N. ophidion females were not choosy at all.

The Measurement of Sexual Selection Using Bateman's Principles: An Experimental Test in the Sex-Role-Reversed Pipefish Syngnathus typhle

Abstract Angus J. Batemans classic study of sexual selection in Drosophila melanogaster has had a major influence on the development of sexual selection theory. In some ways, Batemans study has served a catalytic role by stimulating debate on sex roles, sexual conflict and other topics in sexual selection. However, there is still considerable disagreement regarding whether or not “Batemans principles” are helpful in the study of sexual selection. Here, we test the idea that Batemans principles provide the basis for a useful method to quantify and compare mating systems. In this study, we focus on the sex-role-reversed pipefish Syngnathus typhle as a model system to study the measurement of sexual selection. We set up artificial breeding assemblages of pipefish in the laboratory and used microsatellite markers to resolve parentage. Three different sex-ratio treatments (female-biased, even and male-biased) were used to manipulate the expected intensity of sexual selection. Measures of the mating system based on Batemans principles were calculated and compared to the expected changes in the intensity of sexual selection. We also compare the results of this study to the results of a similar study of Batemans principles in the rough-skinned newt, a species with conventional sex roles. The results of this experiment show that measures of the mating system based on Batemans principles do accurately capture the relative intensities of sexual selection in the different treatments and species. Thus, widespread use of Batemans principles to quantify mating systems in nature would facilitate comparative studies of sexual selection and mating system evolution.

Male and female mate choice affects offspring quality in a sex-role-reversed pipefish.

Where both sexes invest substantially in offspring, both females and males should discriminate between potential partners when choosing mates. The degree of choosiness should relate to the costs of choice and to the potential benefits to be gained. We measured offspring quality from experimentally staged matings with preferred and non–preferred partners in a sex–role–reversed pipefish, Syngnathus typhle L. Here, a substantial male investment in offspring results in a lower potential reproductive rate in males than in females, and access to males limits female reproductive success rather than vice versa. Thus, males are choosier than females and females compete more intensely over mates than do males. Broods from preferred matings were superior at escaping predation, when either males or females were allowed to choose a partner. However, only ‘choosing’ females benefited in terms of faster–growing offspring. Our results have important implications for mate–choice research: here we show that even the more competitive and less choosy sex may contribute significantly to sexual selection through mate choice.

Male limitation of female reproductive success in a pipefish: effects of body-size differences

SummaryIn the pipefish Syngnathus typhle, a species with exclusive male parental care, males limit female reproductive success because of their limited brood pouch space and long pregnancy. Sexual size dimorphism is absent in these 1-year-old animals but increases with age so that older females are larger than similarly aged males. Because fecundity is related to size in both sexes and increases more rapidly with body size in females than in males, the difference in growth increases female fecundity more, relative to male fecundity, as the fish get older. We therefore predicted that male limitation of female reproductive success is even more severe when all age classes are considered. To measure a females maximum reproductive rate, she was provided with three males. Small 1-year-old females produced as many eggs, or produced eggs at the same rate, as a male of similar size could care for. Small females filled on average 1.06 males within the time span of one male pregnancy and actually produced on average 10 eggs fewer than needed to fill a similarly sized male. Large 2-year-old females, in contrast, produced on average a surplus of 149 eggs and filled 2.7 similarly sized males within the course of one pregnancy. The difference between females of the two size classes was highly significant. Males prefer to mate with larger females if given a choice. In nature sex ratios are equal, and males limit female reproductive success in the whole population. Therefore, small females are more severely constrained by mate availability than are larger females because males choose to mate with larger females.

Male avoidance of parasitized females explained by direct benefits in a pipefish

Abstract The influence of the parasitic trematode,Cryptocotylesp., on male mate choice in a species of pipefish,Syngnathus typhle, was studied. This parasite induces visible black spots in the skin of pipefish, but cannot be transmitted directly from one pipefish to another. In a mate-choice experiment the males spent more time with females with few or no black spots than with females with many black spots. This result was obtained in experiments with natural variation in parasite load, and also in experiments in which black spots were manipulated using tattoo ink. This suggests that males discriminate against parasitized females by using visual cues. In another choice experiment, males did not show any preference between males with or without black spots, suggesting that the discrimination occurs only in a sexual context. There was a negative correlation between parasite load and female fecundity. As a result, males mating with unparasitized females may benefit directly by fertilizing more eggs.