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

Department of Biology, University of Konstanz, 78457 Konstanz, Germany.
Evolution (Impact Factor: 4.61). 07/2003; 57(6):1374-86. DOI: 10.1111/j.0014-3820.2003.tb00345.x
Source: PubMed


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.

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    • "Rather, some species of pipefishes and seadragons carry the eggs attached to the ventral surface of the male with no outer covering. In addition, the brood-pouch structure is thought to have evolved at least twice in the Syngnathidae (Wilson et al. 2003; Wilson and Rouse 2010; Wilson and Orr 2011), so it provides an opportunity to study convergent evolution in a phylogenetic context. Thus, the brood pouch of the Family Syngnathidae provides a novel reproductive tissue, which has an interesting evolutionary history and has the potential to contribute to a better understanding of the role of positive selection in the evolution of reproductive proteins. "
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    ABSTRACT: Evolutionary studies have revealed that reproductive proteins in animals and plants often evolve more rapidly than the genome-wide average. The causes of this pattern, which may include relaxed purifying selection, sexual selection, sexual conflict, pathogen resistance, reinforcement, or gene duplication, remain elusive. Investigative expansions to additional taxa and reproductive tissues have the potential to shed new light on this unresolved problem. Here, we embark on such an expansion, in a comparison of the brood-pouch transcriptome between two male-pregnant species of the pipefish genus Syngnathus. Male brooding tissues in syngnathid fishes represent a novel, nonurogenital reproductive trait, heretofore mostly uncharacterized from a molecular perspective. We leveraged next-generation sequencing (Roche 454 pyrosequencing) to compare transcript abundance in the male brooding tissues of pregnant with nonpregnant samples from Gulf (S. scovelli) and dusky (S. floridae) pipefish. A core set of protein-coding genes, including multiple members of astacin metalloprotease and c-type lectin gene families, is consistent between species in both the direction and magnitude of expression bias. As predicted, coding DNA sequence analysis of these putative "male pregnancy proteins" suggests rapid evolution relative to nondifferentially expressed genes and reflects signatures of adaptation similar in magnitude to those reported from Drosophila male accessory gland proteins. Although the precise drivers of male pregnancy protein divergence remain unknown, we argue that the male pregnancy transcriptome in syngnathid fishes, a clade diverse with respect to brooding morphology and mating system, represents a unique and promising object of study for understanding the perplexing evolutionary nature of reproductive molecules.
    Ecology and Evolution 10/2013; 3(12):4092-4108. DOI:10.1002/ece3.763 · 2.32 Impact Factor
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    • "Analogous to Darwin's theory, it could be expected that, in organisms with reversed sex roles, more polyandrous species exhibit higher levels of sexual dimorphism (Jehl and Murray 1986). The study of mating systems in sex-role–reversed species, therefore, provides exceptional opportunities to test predictions of sexual selection theory (Williams 1975; Wilson et al. 2003). "
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    ABSTRACT: Sexual selection theory predicts that, in organisms with reversed sex roles, more polyandrous species exhibit higher levels of sexual dimorphism. In the family Syngnathidae (pipefish, seahorses, and seadragons), males provide all parental care by carrying developing embryos on their ventral surfaces, and females develop secondary sex characters. Syngnathids exhibit a variety of genetic mating patterns, making them an ideal group to test predictions of sexual selection theory. Here, we describe the mating system of the black-striped pipefish Syngnathus abaster, using 4 highly variable microsatellites to analyze parentage of 102 embryos. Results revealed that 1) both sexes mate multiple times over the course of a pregnancy (polygynandrous mating system), 2) eggs are spatially segregated by maternity within each brood pouch, and 3) larger females have higher mating success (Kolmogorov-Smirnov test; P < 0.05). Together with similar studies of other syngnathid species, our results support the hypothesis that the mating system is related to the intensity of sexual dimorphism.
    The Journal of heredity 08/2013; 104(6). DOI:10.1093/jhered/est049 · 2.09 Impact Factor
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    • "The list of species in which males heavily invest in nuptial gifts or in parental care has quickly increased in the last decades, revealing cases of female–female competition for access to males and even exclusive male mate choice (e.g., Wilson et al. 2003; Bain and Govedich 2004a; Wells 2007; Gwynne 2008). Among arthropods, exclusive paternal care "
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    ABSTRACT: Paternal care has independently evolved in several arthropod lineages, but mating interactions have been described in detail for only a few species. Here, we describe the mating behavior of Iporangaia pustulosa, a Neotropical harvestman with exclusive paternal care. We obtained the data under natural conditions, and the results are based on 51 mating interactions. Females performed mate searching exclusively, locating and approaching stationary caring males on the vegetation. Upon arrival, nearly 33 % of the visiting females were promptly attacked and repelled by the males without copulating. We did not observe pre-copulatory courtship, and males, exclusively, performed copulatory courtship. Nearly 30 % of the females that copulated with caring males left the clutches without laying any egg. Finally, several behavioral actions reported here are remarkably similar to those observed in the sex-role-reversed harvestman Zygopachylus albomarginis, for which there is strong evidence of both male and female mate choice. In conclusion, our results provide evidence of male aggressive rejection of mates and female abandonment of clutches without ovipositing, suggesting that individuals of both sexes may evaluate and select mating partners.
    acta ethologica 06/2013; 17(1). DOI:10.1007/s10211-013-0152-6 · 1.00 Impact Factor
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