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Male Pregnancy in Seahorses and Pipefishes (Family Syngnathidae): Rapid Diversification of Paternal Brood Pouch Morphology Infer

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Male Pregnancy in Seahorses and Pipefishes (Family Syngnathidae): Rapid Diversification of Paternal Brood Pouch Morphology Infer Male Pregnancy in Seahorses and Pipefishes (Family Syngnathidae): Rapid Diversification of Paternal Brood Pouch Morphology Inferred From a Molecular Phylogeny A. B. Wilson, A. Vincent, I. Ahnesjo¨ , and A. Meyer In contrast to the majority of vertebrate species, primary male parental care is common in fishes and encompasses a remarkable diversity of adaptations. Seahorses and pipe- fishes (Family Syngnathidae) exhibit some of the most specialized forms of paternal care in animals and so are ideally suited to the study of the evolution of male parental care. During mating, female syngnathids transfer eggs to specialized morphological structures that are located on either the abdomen or tail of the male. The male provides all postfertilization parental care and has morphological and physiological adaptations to osmoregulate, aerate, and even nourish the developing embryos. While all syng- nathid species are adapted for paternal care, the brooding structure with which this is accomplished varies between species, from simple ventral gluing areas to much more complex structures such as the completely enclosed pouches of the seahorses. Our combined cytochrome b-, 12S rDNA-, and 16S rDNA-based molecular phylogeny of syngnathid fishes demonstrates that rapid diversification of male brooding structures has been associated with the major evolutionary radiation of the group, suggesting that development and diversification of structures involved in paternal care may have been key evolutionary innovations of the Syngnathidae. Molecular analyses also high- light geographical centers of biodiversity and suggest interoceanic migration of Syng- nathus pipefishes from their center of origin in the Pacific. Evolutionary theory predicts that organisms ald 1959). This key morphological inno- should attempt to maximize reproductive vation ensures a male complete confi- success by monopolizing resources and ma- dence in the paternity of its offspring tes and optimizing costs and benefits of pa- (Jones and Avise 1997; Jones et al. 1999), rental care (Andersson 1994; Clutton-Brock but at a cost of paternal care that exceeds 1991; Darwin 1871; Emlen and Oring 1977). that of most other vertebrates (Clutton- Female parental care far exceeds that of Brock and Vincent 1991). From the Department of Biology, University of Konstanz, Universita¨tstrasse 10, Konstanz 78457, Germany (Wilson males in many vertebrates, but this pattern Primary taxonomic groupings within the and Meyer), Department of Biology, McGill University, is reversed in fishes where, in addition to family Syngnathidae reflect the location Montreal, Quebec, Canada (Vincent), and Department of gametic investment, males often provide the and development of the male brood pouch Animal Ecology, Uppsala University, Uppsala, Sweden (Ahnesjo¨). Thanks to J. C. Avise, S. Lourie, and two anon- majority of parental care (Blumer 1982). (Duncker 1915; Herald 1959) (Figure 1): ymous reviewers for comments on the manuscript. We Fish are exceptional in their wide variety of type B1—eggs are loosely attached to the thank M. A. Bell, W. Chan, C. Dayton, P. Franzoi, R. A. parental care behaviors (Baylis 1981), and ventral side of the male and are completely Fritzsche, J. de Greef, A. Jordan, C. King, F. Leung, C. Linaker, H. Masonjones, R. E. Matheson, G. Orti, D. Rez- have been instrumental in increasing our un- unprotected by a brood pouch (Entelurus, nick, R. Ruiz-Carus, and R. L. Teixeira for assistance with derstanding of the evolutionary origins of Nerophis); types A2 and B2—eggs are collections. We are grateful to J. M. Morrissey, P. J. Perl, and P. A. Ritchie for technical assistance. This work was parental care (Baylis 1981; Gross and Sar- placed into individual membranous egg funded by an NSERC PGSB scholarship (to A.B.W.), re- gent 1985). compartments (Solegnathus, Doryrham- search grants from the Deutsche Forschungsgemein- The order Gasterosteiformes includes phus); type B3—eggs are incubated in a schaft (DFG ME1725/2-1, ME1725/3-1, ME1725/4-1, ME1725/5-1, GL297/1-1), the U.S. National Science Foun- fishes with a remarkable diversity of re- well-defined pouch and protected by pouch dation (BSR-9107838; BSR-9119867, DEB-96-15178), and productive behaviors (Breder and Rosen plates (ventral extensions of the lateral the Fond der Chemischen Industrie (to A.M.), the Ernest 1966; Clutton-Brock and Vincent 1991). plates of the trunk or tail rings) (Oostethus); Cook Research Fellowship from Somerville College, Ox- ford (to A.V.), and funding from the Swedish Natural Sci- The family Syngnathidae (pipefishes and type A4—eggs are placed into a well-de- ence Research Council (to I.A.). Address correspondence seahorses) are characterized by especially fined pouch, with fleshy bilateral pouch to Axel Meyer at the address above or e-mail: [email protected]. This paper was delivered pronounced adaptations for male parental folds that meet on the ventral midline of at a symposium entitled ‘‘DNA-Based Profiling of Mating care, with the female depositing eggs di- the pouch and partially or fully enclose the Systems and Reproductive Behaviors in Poikilothermic rectly to a specialized incubation area or eggs (Syngnathus); type A5—eggs are incu- Vertebrates’’ sponsored by the American Genetic Asso- ciation at Yale University, New Haven, CT, USA, June 17– brood pouch on either the tail (type A: bated in a completely enclosed saclike 20, 2000. subfamily Urophori) or the trunk (type B: fleshy pouch, which opens through an an- ᭧ 2001 The American Genetic Association 92:159–166 subfamily Gastrophori) of the male (Her- teromesial slit or pore (Hippocampus). Al- 159 Figure 1. Hypothetical evolutionary development of the syngnathid brood pouch (Herald 1959), detailing independent radiations of Urophori and Gastrophori and the diversification of pouch types. For descriptions of pouch type variation, see text. Generic names (in italics) represent taxonomic sampling of the present study. Shown are schematic cross sections through the male brood pouch (Herald 1959), showing general pouch design and the extent of pouch enclosure. though neither type A1 or A3 pouch types and evolution of a broad array of animal across the entire geographic range of the are known from the fossil record, the sub- taxa (Avise 2000; Avise et al. 1987) and Syngnathidae (Table 1, Figure 2). Archived families of both the Gastrophori and Uro- have given us a better understanding of syngnathid samples are housed at the phori are hypothesized to have evolved both the approximate timing and relative Evolutionary Biology Center (Uppsala, through successive development of the rates of diversification in many fish spe- Sweden). Specimens used as outgroups brood pouch (Herald 1959; Figure 1). cies (Bermingham et al. 1997; Bernatchez (collection locality) were three members The extreme degree of specialization for and Wilson 1998; Meyer 1993; Meyer et al. of the stickleback family Gasterosteidae paternal care in the Syngnathidae is ac- 1990). In the present study we use frag- [threespine stickleback (Gasterosteus acu- companied by a notable increase in spe- ments of mitochondrial 12S rDNA and 16S leatus), New York; blackspotted stickle- cies-level diversity over that of closely re- rDNA genes and the complete cytochrome back (G. wheatlandii), Rhode Island; and lated groups. The Syngnathidae are by far b mitochondrial gene to clarify syngnathid ninespine stickleback (Pungitius pungitius), the most diverse family in the order Gas- phylogeography and investigate the evo- Scotland], and the Japanese tubenose (Au- terosteiformes, with approximately 230 lution of morphological specializations for lichthys japonicus) (Kanagawa, Japan), a described species (Dawson 1985), while paternal care in the Syngnathidae. member of the family Aulorhynchidae. their close relative, the stickleback family, Previous morphology-based taxonomic is comprised of only 7 species (Wootton revisions of the family have stressed the DNA Extraction/mtDNA Sequencing 1984). However, whereas most species of importance of the male brood pouch in Specimens were preserved in 70% ethanol the syngnathid radiation and have made sticklebacks have a circumpolar distribu- and total genomic DNA was extracted male reproductive biology a key taxonom- tion concentrated in the northern hemi- from white muscle or liver tissue by pro- ic character in defining the group (Daw- sphere (Wootton 1984), the highest diver- teinase K/SDS digestion and purified by son 1985; Duncker 1915; Herald 1959). Our sity of the syngnathids is concentrated in phenol-chloroform extraction and ethanol molecular investigation investigates this a relatively small region of the southwest precipitation (Kocher et al. 1989). Frag- assumption with a suite of three mito- Pacific (Dawson 1985). As the Gasterostei- chondrial gene fragments. Strong congru- ments of 12S rDNA and 16S rDNA genes dae are believed to be closely related to ency between Herald’s (1959) proposed and the complete cytochrome b gene were the Syngnathidae (Bowne 1984), this strik- model of paternal care evolution and the polymerase chain reaction (PCR) ampli- ing difference in both species-level diver- present molecular phylogenetic study fied with primers under previously pub- sity and geographic distribution is partic- would provide support for the significance lished reaction conditions (Table 2). Ap- ␮ ularly notable. Evidently lineage-specific of brood pouch diversification on the evo- proximately 0.2 g of QIAquick (Qiagen) factors have been responsible for the lution of these fishes. Alternatively,
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