Reversed sex roles and parental energy investment in zygotes of two pipefish (Syngnathidae) species

Berglund, Anders; Rosenqvist, Gunilla; Svensson, Ingrid

doi:10.3354/meps029209

Cited by 176 publications

(168 citation statements)

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“…embryonic stage) did not influence male ventilation rates or activity patterns. However, since embryonic metabolic demands tend to peak just before hatching [8,46,67,[83][84][85], it is possible that hypoxia impacts embryo survival only towards the end of the brooding period.…”

Section: (C) Paternal Carementioning

confidence: 99%

“…As is typical for many pipefishes and seahorses (Syngnathidae), males of this genus care for the developing embryos in a sealed brood pouch where they protect, osmoregulate, oxygenate and transfer nutrients to the embryos through the vascularized walls of the pouch [37,[42][43][44][45]. Moreover, previous work on S. typhle has shown that larger embryos have higher respiration rates than smaller ones [46], larger eggs result in larger offspring [47] and that larger juveniles enjoy fitness benefits [48].…”

Section: Introductionmentioning

confidence: 99%

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The evolutionary puzzle of egg size, oxygenation and parental care in aquatic environments

2015

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Offspring fitness generally improves with increasing egg size. Yet, eggs of most aquatic organisms are small. A common but largely untested assumption is that larger embryos require more oxygen than they can acquire through diffusion via the egg surface, constraining egg size evolution. However, we found no detrimental effects of large egg size on embryo growth and survival under hypoxic conditions. We tested this in the broad-nosed pipefish, Syngnathus typhle, whose males provide extensive care (nourishment, osmoregulation and oxygenation) to their young in a brood pouch on their bodies. We took advantage of this species' pronounced variation in egg size, correlating positively with female size, and tested the effect of hypoxia (40% dissolved oxygen) versus fully oxygenated (100%) water on embryo size and survival of large versus small eggs after 18 days of paternal brooding. Egg size did not affect embryo survival, regardless of O 2 treatment. While hypoxia affected embryo size negatively, both large and small eggs showed similar reductions in growth. Males in hypoxia ventilated more and males with large eggs swam more, but neither treatment affected their position in the water column. Overall, our results call into question the most common explanation for constrained egg size evolution in aquatic environments.

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Section: (C) Paternal Carementioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The evolutionary puzzle of egg size, oxygenation and parental care in aquatic environments

2015

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“…Seahorses, as members of the Syngnathidae family of fishes, exhibit the characteristic reproductive trait of this family: advanced paternal care of the developing embryos (Berglund et al 1986;Vincent 1990;Vincent et al 1992;Lourie et al 1999;Wilson et al 2001). The male seahorse receives the eggs from the female into his enclosed brood pouch where they remain post-fertilisation until the fully developed and independent juveniles are released.…”

Section: Introductionmentioning

confidence: 99%

Reproductive output of male seahorses,Hippocampus abdominalis,from Wellington Harbour, New Zealand: Implications for conservation

Woods¹

2005

New Zealand Journal of Marine and Freshwater Research

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This investigation examines aspects of reproductive output in brooding wild male seahorses, Hippocampus abdominalis, from Wellington Harbour, New Zealand. Previously undocumented, such information is crucial to the management and protection of this species in relation to the CITES Appendix II-listing of all seahorse species. Brooding males (n = 46) were captured and kept captive until the release of their juveniles, whereupon the number of juveniles was counted and sampled for standard length (SL) and dry weight (DW). SL (mean ± 1SE) of brooding males was 18.1 ± 0.6 cm and wet weight (WW) 17.6 ± 1.6 g. Number (mean ± 1SE) of juveniles released per brood was 271.2 ± 27. The number of juveniles produced was positively correlated with parent SL, WW, and brood pouch volume. Brood pouch volume was positively correlated with male SL. SL (mean ±1SE) of juveniles released was 16.7 + 0.2 mm and DW 1.2 ± 0.1 mg. Mean SL and DW of juveniles were not correlated with the number of juveniles per brood, parent male SL or parent male pouch volume. The percentage of pouch contents which were non-viable (i.e., premature or non-viable eggs) upon juvenile release was low (1.1 ± 0.2%; mean ±1SE of the total pouch contents). Based on findings in this study it is suggested that the CITES 10 cm minimum height restriction, which can be used in lieu of non-detriment findings to allow sustainable exploitation of seahorses, is not suitable for H. abdominalis from Wellington Harbour as it would appear to only protect small males that produce low numbers of juveniles.

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“…However, in many cases, time and energy expenditures may be positively correlated and, in general, a large expenditure will often carry larger costs and therefore represent a higher parental investment. In the limited number of syngnathids studied to date, males of species with less complex brooding structures (e.g., Nerophis ophidion) spend less energy on their young than do those brooding embryos in enclosed pouches with placentalike structures (e.g., Hippocampus zosterae, Syngnathus typhle; Berglund et al 1986;Masonjones 2001). If increasing pouch complexity results in a general increase in male parental investment relative to females, we would expect to see more frequent sex-role reversals in species with more complex brood pouches.…”

mentioning

confidence: 99%

“…This evolutionary innovation ensures males complete confidence of paternity (Jones and Avise 1997;Jones et al 1998Jones et al , 1999, but at a level of paternal investment that exceeds that of most other vertebrates (Breder and Rosen 1966). Thereafter the embryos are nourished, osmoregulated, and protected during a lengthy period of male pregnancy (Berglund et al 1986(Berglund et al , 1989Vincent et al 1992). The brooding structures vary in complexity in five steps, from: (1) a simple unprotected ventral area for gluing, (2) individual membranous egg compartments, (3) protection of eggs in a pouch with pouch plates, (4) bilateral pouch folds that grow together into a closed pouch, to (5) the most complex and completely enclosed brooding pouch of seahorses (Dawson 1985).…”

mentioning

confidence: 99%

The Dynamics of Male Brooding, Mating Patterns, and Sex Roles in Pipefishes and Seahorses (Family Syngnathidae)

et al. 2003

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Abstract. 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 likelihoodbased 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. In the vast majority of animals, the male's sole contribution to his offspring is his sperm (Trivers 1972). As a result, even when the observed sex ratio of males to females is equal, the operational sex ratio is often biased toward males and males almost universally compete more strongly for mates, while females typically exert greater mate choice (Darwin 1871;Emlen and Oring 1977). Although most egg-laying fishes leave their eggs unprotected after spawning, sole male care is the predominant pattern in those species that care for their young (Blumer 1982). Paternal care is likely to increase offspring fitness, but may reduce the father's ability to invest in other offspring (i.e., a parental investment sensu Trivers 1972).Sex roles are defined by mating competition (Emlen and Oring 1977). Sex-role reversal occurs when females primarily compete for access to mates, as compared to conventional sex roles with male-male mating competition (cf. mating roles, Gwynne 1991). Traditionally, the concept of parental investment has been us...

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Reversed sex roles and parental energy investment in zygotes of two pipefish (Syngnathidae) species

Cited by 176 publications

References 10 publications

The evolutionary puzzle of egg size, oxygenation and parental care in aquatic environments

The evolutionary puzzle of egg size, oxygenation and parental care in aquatic environments

Reproductive output of male seahorses,Hippocampus abdominalis,from Wellington Harbour, New Zealand: Implications for conservation

The Dynamics of Male Brooding, Mating Patterns, and Sex Roles in Pipefishes and Seahorses (Family Syngnathidae)

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