Transient ontogenetic expression of hermaphroditic gonad morphology within the Gobiosoma group of the Neotropical seven-spined gobies (Teleostei: Gobiidae)
Tóm tắt
The Neotropical seven-spined gobies (tribe Gobiosomatini), including the Gobiosoma and Microgobius groups, constitute a speciose, monophyletic gobiid taxon. In particular, member species of the Gobiosoma group exhibit a combination of behavioral diversification and microhabitat specialization that may have played a major role in their collective rapid evolution and high rate of speciation. Functional hermaphroditism, which is common among gobiids, can promote exploitation of patchily distributed micro-niches by countering potential reductions in reproductive opportunities. However, the possible role of functional hermaphroditism in the exploitation of microhabitats and rapid speciation in the Gobiosoma group is unknown. One member species, Tigrigobius multifasciatus, is a functional hermaphrodite. Two other Gobiosoma group species are functionally gonochoric (i.e., constant-sexed), but exhibit transient hermaphroditic ovarian structure among immatures. In this study, ovarian morphology among immature and adult females of several Gobiosoma group species was examined to see if hermaphroditic gonadal features are present. Although no evidence of functional hermaphroditism in the form of precursive accessory gonadal structures (pAGS) associated with the adult ovary was found among newly examined species, all species exhibited the transient expression of hermaphroditic gonadal features associated with the immature ovary. In contrast, among six species of non-Gobiosomatini genera having no record of hermaphroditism, none exhibited similar transient hermaphroditic features associated with the immature ovary. These findings suggest that hermaphroditism may have been an ancestral trait which has been secondarily lost within some Gobiosoma group species. This study also shows that ontogenetic and morphogenic processes within the gobiid reproductive system may provide new insights into the evolution of life history traits and significantly further our understanding of the extraordinary evolutionary success of this group.
Tài liệu tham khảo
Birdsong RS, Robins CR (1995) New genus and species of the seven-spined goby (Gobiidae: Gobiosomini) from the offing of the Amazon River, Brazil. Copeia 1995:676–683
Burns JR, Weitzman SH, Grier HJ, Menezes NA (1995) Internal fertilization, testis and sperm morphology in glandulocaudinae fishes (Teleostei: Characidae: Glandulocaudinae). J Morphol 224:131–14
Cole KS (1983) Protogynous hermaphroditism in a temperate zone territorial marine goby, Coryphopterus nicholsi. Copeia 1983:809–812
Cole KS (1988) Predicting the potential for sex-change on the basis of ovarian structure in gobiid fishes. Copeia 1988:1082–1086
Cole KS (1990) Patterns of gonad structure in hermaphroditic gobies. Environ Biol Fishes 28:125–142
Cole KS (2002) Gonad morphology, sexual development, and colony composition in the obligate coral-dwelling damselfish Dascyllus aruanus. Mar Biol 140:151–163
Cole KS (2003) Hermaphroditic characteristics of gonad morphology and inferences regarding reproductive biology in Caracanthus (Teleostei, Scorpaeniformes). Copeia 2003:68–80
Cole KS, Hoese DF (2001) Gonad morphology, colony demography and evidence for hermaphroditism in Gobiodon okinawae (Teleostei, Gobiidae). Environ Biol Fishes 61:161–173
Cole KS, Robertson DR (1988) Protogyny in the Caribbean reef goby, Coryphopterus personatus: gonad ontogeny and social influences on sex change. Bull Mar Sci 42:317–333
Cole KS, Robertson DR, Cedeno AA (1994) Does gonad structure reflect sexual pattern in all gobiid fishes? Environ Biol Fishes 41:301–309
Cole KS, Shapiro DY (1990) Gonad structure and hermaphroditism in the gobiid genus Coryphopterus (Teleostei: Gobiidae). Copeia 1990:996–1003
Cole KS, Shapiro DY (1992) Gonadal structure and population characteristics of the protogynous goby Coryphopterus glaucofraenum. Mar Biol 113:1–9
Colin PL (1975) The neon gobies: comparative biology of the gobies of the genus Gobiosoma, subgenus Elacatinus, (Pisces: Gobiidae) in the tropical western Atlantic. T.F.H. Publications, Neptune
Colin PL (2002) A new species of sponge-dwelling Elacatinus (Pisces: Gobiidae) from the western Caribbean. Zootaxa 106:1–7
Grier HJ, Parenti LR (1994) Reproductive biology and systematics of phallostethid fishes as revealed by gonad structure. Environ Biol Fishes 41:287–299
Jewett SL, Lachner EA (1983) Seven new species of the Indo-Pacific genus Eviota (Pisces: Gobiidae). Proc Biol Soc Washington 96:780–806
Kobayashi Y, Sunobe T, Kabayashi T, Nagahama Y (2005) Gonadal structure of the serial-sex changing gobiid fish Trimma okinawae. Dev Growth Differ 47:7–13
Kuwamura T, Nakashima Y, Yogo Y (1994) Sex change in either direction by growth rate advantage in a monogamous coral goby Paragobiodon echinocephalus. Behav Ecol 5:434–438
Lassig BR (1977) Socioecological strategies adopted by obligate coral-dwelling fishes. Proc Third Int Coral Reef Symp I:565–570
Miller PJ (1984) The tokology of gobioid fishes. In: Potts GW, Wootton RJ (eds) Fish reproduction: strategies and tactics. Academic Press, London, pp 119–153
Miller PJ (1986) Reproductive biology and systematic problems in gobioid fishes. In: Uyeno T, Arai R, Taniuchi T, Matsuura K (eds) Indo-Pacific fish biology. Tokai Univ Press, Tokyo, pp 640–647
Miller PJ (1992) The sperm duct gland: a visceral synapomorphy for gobioid fishes. Copeia 1992:253–256
Munday PL, Caley MJ, Jones GP (1998) Bi-directional sex change in a coral-dwelling goby. Behav Ecol Sociobiol 43:371–377
Nakashima Y, Kuwamura T, Yogo Y (1996) Both-ways sex change in monogamous coral gobies, Gobiodon spp. Environ Biol Fishes 46:281–288
Parenti LR, Song J (1996) Phylogenetic significance of the pectoral/pelvic fin association in acanthomorph fishes: a reassessment using comparative neuroanatomy. In: Stiassny MLJ, Parenti LR, Johnson GD (eds) Interrelationships of fishes. Academic Press, San Diego, pp 427–444
Parenti LR, Grier H (2004) Evolution and phylogeny of gonad morphology in bony fishes. Integr Compar Biol 44:333–348
Robertson DR, Justines G (1982) Protogynous hermaphroditism and gonochorism in four Caribbean reef gobies. Environ Biol Fishes 7:137–142
Rüber L, Van Tassell JL, Zardoya R (2003) Rapid speciation and ecological divergence in the American seven-spined gobies (Gobiidae, Gobiosomatini) inferred from a molecular phylogeny. Evolution 57:1584–1598
Song J, Boord RL (1993) Motor components of the trigeminal nerve and organization of mandibular arch muscles: phylogenetic conservative patterns and their ontogenetic basis. Symposium proceeding for the “Structure, Development and Phylogeny of Cranial Nerves”, ASZ, 1991. Acta Anatomica 148:139–149
Song J, Parenti LR (1995) Clearing and staining whole fish specimens for simultaneous demonstration of bone, cartilage, and nerves. Copeia 1995:114–118
Sponaugle S, Cowen RK, Shanks A, Morgan SG, Leis JM, Pineda J, Boehlert GW, Kingsford MJ, Lindeman KC, Grimes C, Munro JL (2002) Predicting self-recruitment in marine populations: biophysical correlates and mechanisms. Bull Mar Sci 70:341–375
St Mary CM (1993) Novel sexual patterns in two simultaneously hermaphroditic gobies, Lythrypnus dalli and Lythrypnus zebra. Copeia 1993:1062–1072
St Mary CM (1998) Characteristic gonad structure in the gobiid genus Lythrypnus with comparisons to other hermaphroditic gobies. Copeia 1998:720–724
St Mary CM (2000) Sex allocation in Lythrypnus (Gobiidae): variations on a hermaphroditic theme. Environ Biol Fishes 58:321–333
Sunobe T, Nakazono A (1993) Sex change in both directions by alteration of social dominance in Trimma okinawae (Pisces: Gobiidae). Ethology 94:339–345
Sunobe T, Nakazono A (1999) Mating system and hermaphroditism in the gobiid fish, Priolepis cincta, at Kagoshima, Japan. Ichthyol Res 46:103–105
Swearer SE, Shima JS, Hellberg ME, Thorrold SR, Jones GP, Robertson DR, Morgan SG, Selkoe KA, Ruiz GM, Warner RR (2002) Evidence of self-recruitment in demersal marine populations. Bull Mar Sci 70:251–271
Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299:107–109
Taylor MS, Hellberg ME (2005) Marine radiations at small geographic scales: speciation in neotropical reef gobies (Elacatinus). Evolution 59:374–385
Thacker CE, Cole KS (2002) Phylogeny and evolution of the gobiid genus Coryphopterus. Bull Mar Sci 70:837–850
Wallace RA, Selman K (1981) Cellular and dynamic aspects of oocyte growth in teleosts. Am Zool 21:325–343
Wallace RA, Selman K (1990) Ultrastructural aspects of oogenesis and oocyte growth in fish and amphibians. J Electron Micro Tech 16:175–201
Winterbottom R, Southcott S (2007) Two new species of the genus Trimma (Percomorpha: Gobiidae) from western Thailand. Aqua 13:69–76
Winterbottom R, Zur M (2007) Three new species of genus Trimma from Palau, Western Pacific (Percomorpha: Gobiidae). Aqua 13:13–24
