54
Views
1
CrossRef citations to date
0
Altmetric
Original Articles

Group Sex, Sex Change, and Parasitic Males: Sexual Strategies among the Fishes and Their Neurobiological Correlates

&
Pages 160-184 | Published online: 15 Nov 2012

References

  • Acher , R. and Chauvet , J. 1988 . Structure, processing and evolution of the neurohypophyseal hormone-neurophysin precursors . Biochemie , 70 : 1197 – 1207 .
  • Almada , V. C. , Goncalves , E. J. , Oliveira , R. F. and Santos , A. J. 1995 . Courting females: Ecological constraints affect sex roles in a natural population of the blenniid fish Salaria pavo . Animal Behaviour , 49 : 1125 – 1127 .
  • Andersson , M. 1994 . Sexual selection , Princeton : Princeton University Press .
  • Baker , R. R. and Bellis , M. A. 1995 . Human sperm competition: Copulation, masturbation and infidelity , New York : Chapman & Hall .
  • Bass , A. H. 1992 . Dimorphic male brains and alternative reproductive tactics in a vocalizing fish . Trends in Neuroscience , 15 : 139 – 145 .
  • Bass , A. H. 1993 . From brains to behaviour: Hormonal cascades and alternative mating tactics in teleost fishes . Reviews in Fish Biology and Fisheries , 3 : 181 – 186 .
  • Bass , A. H. 1996 . Shaping brain sexuality . American Scientist , 84 : 352 – 363 .
  • Bass , A. H. and Andersen , K. 1991 . Inter- and intrasexual dimorphisms in vocal control system of a teleost fish: Motor axon number and site . Brain, Behavior and Evolution , 37 : 204 – 214 .
  • Behrents , K. C. 1983 . The comparative ecology and interactions between two sympatric gobies Lythrypnus dalli and Lythrypnus zebra , Los Angeles : University of Southern California . Unpublished doctoral dissertation
  • Bertelsen , E. 1951 . The ceratioid fishes: Ontogeny, taxonomy, distribution and biology . Dana Report , 39 : 1 – 281 .
  • Breder , C. M. and Rosen , D. E. 1966 . Modes of reproduction in fishes , Garden City , NY : Natural History Press .
  • Carneiro , L. A. , Oliveira , R. F. , Canário , A. V. M. and Grober , M. S. The effect of arginine vasotocin on courtship behaviour in a blenniid fish with alternative reproductive tactics . Fish Physiology and Biochemistry , (in press)
  • Caro , T. M. and Bateson , P. 1986 . Organization and ontogeny of alternative tactics . Animal Behaviour , 34 : 1483 – 1499 .
  • Castagna , C. , Absil , P. , Foidart , A. and Balthazart , J. 1998 . Systemic and intracerebroventricular injections of vasotocin inhibit appetitive and consummatory components of male sexual behavior in Japanese quail . Behavioral Neuroscience , 112 : 233 – 250 .
  • Cattanach , B. , Iddon , C. , Charlton , H. , Chiappa , S. and Fink , G. 1977 . Gonadotropin-releasing hormone deficiency in a mutant mouse with hypogonadism . Nature , 269 : 338 – 340 .
  • Conover , D. O. 1984 . Adaptive significance of temperature-dependent sex determination in a fish . American Naturalist , 123 : 297 – 313 .
  • Conover , D. O. and Kynard , B. E. 1981 . Environmental sex determination: Interaction of temperature and genotype in a fish . Science , 213 : 577 – 579 .
  • Davis , M. R. and Fernald , R. D. 1990 . Social control of neuronal soma size . Journal of Neurobiology , 21 : 1180 – 1189 .
  • Demski , L. 1984 . The evolution of neuroanatomical substances of reproductive behavior: Sex steroid and LHRH-specific pathways including the terminal nerve . American Zoologist , 24 : 809 – 830 .
  • DeVries , G. J. and Al-Shamma , H. A. 1990 . Sex differences in hormonal response of vasopressin pathways in the rat brain . Journal of Neurobiology , 21 : 686 – 693 .
  • Devlin , R. H. and Nagahama , Y. 2002 . Sex determination and sex differentiation in fish: An overiew of genetic, physiological, and environmental influences . Aquaculture , 208 : 191 – 364 .
  • Dugatkin , L. A. 1992 . Sexual selection and imitation: Females copy the mate choice of others . American Naturalist , 139 : 1384 – 1389 .
  • Dugatkin , L. A. and Godin , J. G. Reversal of female mate choice by copying in the guppy (Poecilia reticulata . Proceedings of the Royal Society of London. Series B, Biological Sciences . pp. 179 – 184 . 249
  • Dugatkin , L. A. and Godin , J. G. J. 1993 . Female mate copying in the guppy (Poecilia reticulata): Age-dependent effects . Behavioral Ecology , 4 : 289 – 292 .
  • Elofsson , U. , Winberg , S. and Francis , R. C. 1997 . Number of preoptic GnRH-immunoreactive cells correlates with sexual phase in a protandrously hermaphroditic fish, the dusky anemonefish (Amphiprion melanopus . Journal of Comparative Physiology , 181 : 484 – 492 .
  • Elofsson , U. O. , Winberg , S. and Nilsson , G. E. 1999 . Relationships between sex and the size and number of forebrain gonadotropin-releasing hormone-immunoreactive neurones in the ballan wrasse (Labrus berggylta), a protogynous hermaphrodite . Journal of Comparative Neurology , 410 : 158 – 170 .
  • Emlen , S. T. and Oring , L. W. 1977 . Ecology, sexual selection, and the evolution of mating systems . Science , 197 : 215 – 223 .
  • Foran , C. M. and Bass , A. H. 1998 . Preoptic AVT immunoreactive neurons of a teleost fish with alternative reproductive tactics . General and Comparative Endocrinology , 111 : 271 – 282 .
  • Foran , C. M. and Bass , A. H. 1999 . Preoptic GnRH and AVT: Axes for sexual plasticity in teleost fish . General and Comparative Endocrinology , 116 : 141 – 152 .
  • Fox , H. E. , White , S. A. , Kao , M. H. and Fernald , R. D. 1997 . Stress and dominance in a social fish . Journal of Neuroscience , 17 : 6463 – 6469 .
  • Francis , R. C. , Soma , K. and Fernald , R. D. Social regulation of the brain-pituitary-gonadal axis . Proceedings of the National Academy of Sciences of the United States of America . pp. 7794 – 7798 . 90
  • Fricke , H. 1979 . Mating system, resource defence and sex change in the anemonefish Amphiprion akallopisos . Zeitschrift fur Tierpsychologie , 50 : 313 – 326 .
  • Gage , M. G. J. , Stockley , P. and Parker , G. A. 1995 . Effects of alternative male mating strategies on characteristics of sperm production in the Atlantic salmon (Salmo salar): Theoretical and empirical investigations . Philosophical Transactions of the Royal Society of London , 350 : 391 – 399 .
  • Ghiselin , M. T. 1969 . The evolution of hermaphroditism among animals . Quarterly Review of Biology , 44 : 189 – 208 .
  • Godwin , J. , Crews , D. and Warner , R. R. Behavioural sex change in the absence of gonads in a coral reef fish . Proceedings of the Royal Society of London. Series B, Biological Sciences . pp. 1683 – 1688 . 263
  • Godwin , J. , Sawby , R. , Warner , R. R. , Crews , D. and Grober , M. S. 2000 . Hypothalamic arginine vasotocin mRNA abundance variation across sexes and with sex change in a coral reef fish . Brain, Behavior and Evolution , 55 : 77 – 84 .
  • Goncalves , E. J. , Almada , V. C. , Oliveira , R. F. and Santos , A. J. 1996 . Female mimicry as a mating tactic in males of the Blenniid Fish (Salaria pavo . Journal of the Marine Biological Association of the United Kingdom , 76 : 529 – 538 .
  • Goodson , J. L. and Bass , A. H. 2000 . Forebrain peptides modulate sexually polymorphic vocal circuitry . Nature , 403 : 769 – 772 .
  • Goodson , J. L. and Bass , A. H. 2001 . Social behavior functions and related anatomical characteristics of vasotocin/vasopressin systems in vertebrates . Brain Research Reviews , 35 : 246 – 265 .
  • Grober , M. S. 1997 . “ Conserved neuroendocrine foundations give rise to diverse sexual phenotypes in fish ” . In Sexual orientation: Toward biological understanding , Edited by: Ellis , L. and Ebertz , L. 2 – 20 . Westport , CT : Praeger .
  • Grober , M. S. 1998 . Socially controlled sex change: Integrating ultimate and proximate levels of analysis . Acta Ethologica , 1 : 3 – 17 .
  • Grober , M. S. and Bass , A. H. 1991 . Neuronal correlates of sex/role change in labrid fishes: LHRH-like immunoreactivity . Brain, Behavior and Evolution , 38 : 302 – 312 .
  • Grober , M. S. , Fox , S. H. , Laughlin , C. and Bass , A. H. 1994 . GnRH cell size and number in a teleost fish with two male reproductive morphs: Sexual maturation, final sexual status and body size allometry . Brain, Behavior and Evolution , 43 : 61 – 78 .
  • Grober , M. S. , George , A. A. , Watkins , K. K. , Carneiro , L. A. and Oliveira , R. F. 2002 . Forebrain AVT and courtship in a fish with male alternative reproductive tactics . Brain Research Bulletin , 57 : 423 – 425 .
  • Grober , M. S. and Sunobe , T. 1996 . Serial adult sex change involves rapid and reversible changes in forebrain neurochemistry . Neuroreport , 7 : 2945 – 2949 .
  • Gross , M. R. 1991 . Evolution of alternative reproductive stategies: Frequency-dependent sexual selection in male bluegill sunfish . Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences , 332 : 59 – 66 .
  • Halpern-Sebold , L. R. , Schreibman , M. P. and Margolis-Nunno , H. 1986 . Differences between early-and late-maturing genotypes of the platyfish (Xiphophorus maculatus) in the morphometry of their immunoreactive luteinizing hormone releasing hormone-containing cells: A developmental study . Journal of Experimental Zoology , 240 : 245 – 257 .
  • Harrington , R. W. 1975 . “ Sex determination and differentiation among uniparental homozygotes of the hermaphroditic fish Rivulus marmoratus (Cyprinodontidae: Atheriniformes) ” . In Intersexuality in the animal kingdom , Edited by: Reinbotz , R. 249 – 262 . New York : Springer-Verlag .
  • Henson , S. A. and Warner , R. R. 1997 . Male and female alternative reproductive behaviors in fishes: A new approach using intersexual dynamics . Annual Review of Ecology and Systematics , 28 : 571 – 592 .
  • Hoar , W. S. 1988 . “ The physiology of smolting salmonids ” . In Fish Physiology , Edited by: Hoar , W. S. and Randall , D. J. Vol. XI , 275 – 343 . New York : Academic Press .
  • Jenkins , R. E. and Jenkins , D. J. 1980 . Reproductive behavior of the greater redhorse, Moxostoma valenciennesi, in the Thousand Islands Region . Canadian Field-Naturalist , 94 : 426 – 430 .
  • Jones , A. G. , Walker , D. , Kvarnemo , C. , Lindstrom , K. and Avise , J. C. How cuckoldry can decrease the opportunity for sexual selection: Data and theory from a genetic parentage analysis of the sand goby, Pomatoschistus minutus . Proceedings of the National Academy of Sciences of the United States of America . pp. 9151 – 9156 . 99
  • Kallman , K. D. and Schreibman , M. P. 1973 . A sex-linked gene controlling gonadotrop differentiation and its significance in determining the age of sexual maturation and size of the platyfish . Xiphophorus maculatus. General and Comparative Endocrinoogy , 21 : 287 – 304 .
  • Laland , K. N. and Williams , K. 1997 . Shoaling generates social learning of foraging information in guppies . Animal Behaviour , 53 : 1161 – 1169 .
  • Livne , I. , Gibson , M. J. and Silverman , A.-J. 1992 . Brain grafts of migratory GnRH cells induce gonadal recovery in hypogonadal (hpg) mice . Developmental Brain Research , 69 : 117 – 123 .
  • Livne , I. , Silverman , A.-J. and Gibson , M. J. 1992 . Reversal of reproductive deficiency in the hpg male mouse by neonatal androgenization . Biology of Reproduction , 47 : 561 – 567 .
  • Magnhagen , C. 1992 . Alternative reproductive behavior in the common goby, Pomatoschistus microps: An ontogenic gradient . Animal Behaviour , 44 : 182 – 184 .
  • Mason , A. J. , Pitts , S. L. , Nikolics , K. , Szonyi , E. , Wilcox , J. N. Seeburg , P. H. 1986 . The hypogonadal mouse: Reproductive functions restored by gene therapy . Science , 234 : 1372 – 1378 .
  • McIntyre , K. K. 1998 . Arginine vasotocin in the preoptic area of the bluehead wrasse and the effects of 11-ketotestosterone , Tempe : Arizona State University . Unpublsihed master's thesis
  • Metcalfe , N. B. , Huntingford , F. A. , Graham , W. D. and Thorpe , J. E. Early social status and the development of life-history strategies in Atlantic salmon . Proceedings of the Royal Society of London . pp. 7 – 19 . 236
  • Moore , F. L. 1992 . Evolutionary precedents for behavioral actions of oxytocin and vasopressin . Annals of the New York Academy of Sciences , 652 : 156 – 165 .
  • Moore , F. L. and Miller , L. J. 1982 . Arginine vasotocin induces sexual behavior of newts by acting on cells in the brain . Peptides , 4 : 97 – 102 .
  • Muske , L. E. 1993 . Evolution of gonadotropin-releasing hormone (GnRH) neuronal systems . Brain, Behavior and Evolution , 42 : 215 – 230 .
  • Nakamura , M. , Specker , J. and Nagahama , Y. 1996 . Innervation of steroid-producing cells in the ovary of tilapia Oreochromis niloticus . Zooogical Science , 13 : 603 – 608 .
  • Nakashima , Y. , Kuwamura , T. and Yogo , Y. 1995 . Why be a both-ways sex changer? . Ethology , 101 : 301 – 307 .
  • Nakashima , Y. , Kuwamura , T. and Yogo , Y. 1996 . Both-ways sex change in monogamous coral gobies, Gobiodon spp . Environmental Biology of Fishes , 46 : 281 – 288 .
  • Nelson , J. S. 1994 . Fishes of the world , New York : Wiley .
  • Oliveira , R. F. , Canario , A. V. M. and Grober , M. S. 2001 . Male sexual polymorphism, alternative reproductive tactics, and androgens in combtooth blennies (Pisces: Blenniidae . Hormones and Behavior , 40 : 266 – 275 .
  • Page , L. M. and Johnston , C. E. 1990 . Spawning in the creek chubsucker, Erimyzon oblongus, with a review of spawning behavior in suckers (Catostomidae) . Environmental Biology of Fishes , 27 : 265 – 272 .
  • Petersen , C. W. 1995 . Reproductive behavior, egg trading, and correlates of male mating success in the simultaneous hermaphrodite . Serranus tabacarius. Environmental Biology of Fishes , 43 : 351 – 361 .
  • Perez , F. , Fuenzalida , A. , Mendez , E. and Cerisola , H. 1983 . Myoid and leydig-type interstitial cells are simultaneously innervated in the testes of the clingfish Sicyases sanguineus (Teleostei) . Archives de Biologia y Medicina Experimentales , 16 : 177
  • Pfaff , D. W. , Schwanzel-Fukuda , M. , Parhar , I. S. , Lauber , A. H. , McCarthy , M. M. and Kow , L.-M. 1994 . GnRH neurons and other cellular and molecular mechanisms for simple mammalian reproductive behaviors . Recent Progress in Hormone Research , 49 : 1 – 25 .
  • Piferrer , F. 2001 . Endocrine sex control strategies for the feminization of teleost fish . Aquaculture , 197 : 229 – 281 .
  • Pilastro , A. , Scaggiante , M. and Rasotto , M. B. Individual adjustment of sperm expenditure accords with sperm competition theory . Proceedings of the National Academy of Sciences of the United States of America . pp. 9913 – 9915 . 99
  • Policansky , D. 1982 . Sex change in plants and animals . Annual Review of Ecology and Systematics , 13 : 471 – 495 .
  • Pough , F. H. , Heiser , J. B. and McFarland , W. N. 1996 . Vertebrate life , Upper Saddle River , NJ : Prentice Hall .
  • Reavis , R. H. and Grober , M. S. 1999 . An integrative model of sex change: Social, behavioural and neurochemical changes in Lythrypnus dalli (Pisces) . Acta Ethologica , 2 : 51 – 60 .
  • Reighard , J. 1920 . The breeding behaviors of the suckers and minnows. I. The suckers . Biological Bulletin , 38 : 1 – 33 .
  • Rowe , S. and Hutchings , J. A. 2003 . Mating systems and the conservation of commercially exploited marine fish . Trends in Ecology and Evolution , 18 : 567 – 572 .
  • Ryan , M. and Causey , B. A. 1989 . “Alternative” mating behavior in the swordtails Xiphophorus nigrensis and Xiphophorus pygmaeus (Pisces: Poeciliidae) . Behavioral Ecology and Sociobiology , 24 : 341 – 348 .
  • Ryan , M. J. , Hews , D. K. and Wagner , W. E. 1990 . Sexual selection on alleles that determine body size in the swordtail Xiphophorus nigrensis . Behavioral Ecology and Sociobiology , 26 : 231 – 237 .
  • Ryan , M. J. , Pease , C. M. and Morris , M. R. 1992 . A genetic polymorphism in the swordtail Xiphophorus nigrensis: Testing the prediction of equal fitnesses . American Naturalist , 139 : 21 – 31 .
  • Scaggiante , M. , Mazzoldi , C. , Petersen , C. W. and Rasotto , M. B. 1999 . Sperm competition and mode of fertilization in the grass goby Zosterisessor ophiocephalus (Teleostei: Gobiidae) . Journal of Experimental Zoology , 283 : 81 – 90 .
  • Schreibman , M. P. and Kallman , K. D. 1977 . The genetic control of the pituitary-gonadal axis in the platyfish . Xiphophorus maculatus. Journal of Experimental Zoology , 200 : 277 – 294 .
  • Schwanzel-Fukuda , M. , Brick , D. and Pfaff , D. W. 1989 . Luteinizing hormone-releasing hormone (LHRH)-expressing cells do not migrate normally in an inherited hypogonadal (Kallmann) syndrome . Molecular Brain Research , 6 : 311 – 326 .
  • Semsar , K. and Godwin , J. 2003 . Social influences on the arginine vasotocin system are independent of gonads in a sex-changing fish . Journal of Neuroscience , 23 : 4386 – 4393 .
  • Semsar , K. , Kandel , F. L. and Godwin , J. 2001 . Manipulations of the AVT system shift social status and related courtship and aggressive behavior in the bluehead wrasse . Hormones and Behavior , 40 : 21 – 31 .
  • Shapiro , D. Y. 1992 . Plasticity of gonadal development and protandry in fishes . Journal of Experimental Zoology , 261 : 194 – 203 .
  • Sherwood , N. M. , Parker , D. B. , McRory , J. E. and Lescheid , D. W. 1994 . Molecular evolution of growth hormone-releasing hormone and gonadotropin-releasing hormone . Fish Physiology , XIII : 3 – 66 .
  • Silverman , A.-J. , Livne , I. and Witkin , J. 1994 . “ The gonadotropin-releasing hormone (GnRH) neuronal systems: Immunocytochemistry and in situ hybridization ” . In The Physiology of Reproduction, , 2nd ed. , Edited by: Knobil , E. and Neill , J. Vol. 1 , 1683 – 1710 . New York : Raven Press .
  • Silverman , A.-J. and Witkin , J. W. 1994 . Biosynthesis of gonadotropin-releasing hormone during the rat estrous cycle: A cellular analysis . Neuroendocrinology , 59 : 545 – 551 .
  • St. Mary , C. M. 1993 . Novel sexual patterns in two simultaneously hermaphroditic gobies . Lythrypnus dalli and Lythrypnus zebra. Copeia , 4 : 1062 – 1072 .
  • Stockley , P. , Gage , M. J. G. , Parker , G. A. and Moller , A. P. 1997 . Sperm competition in fishes: The evolution of testis size and ejaculate characteristics . American Naturalist , 149 : 933 – 954 .
  • Sunobe , T. and Nakazono , A. 1990 . Polygynous mating system of Trimma okinawae Pisces: Gobiidae) at Kagoshima, Japan with a note on sex change . Ethology , 84 : 133 – 143 .
  • Sunobe , T. and Nakazono , A. 1993 . Sex change in both directions by alteration of social dominance in Trimma okinawae Pisces: Gobiidae . Ethology , 94 : 339 – 345 .
  • Swaab , D. F. and Hofman , M. A. 1990 . An enlarged suprachiasmatic nucleus in homosexual men . Brain Research , 537 : 141 – 148 .
  • Swaab , D. F. , Chung , W. C. J. , Kruijver , P. M. , Hofman , M. A. and Ishunina , T. A. 2001 . Structural and functional sex differences in the human hypothalamus . Hormones and Behavior , 40 : 93 – 98 .
  • Taborsky , M. 1994 . Sneakers, satellites, and helpers: Parasitic and cooperative behavior in fish reproduction . Advances in the Study of Behavior , 23 : 1 – 101 .
  • Taborsky , M. 2001 . The evolution of bourgeois, parasitic, and cooperative reproductive behaviors in fishes . Journal of Heredity , 92 : 100 – 110 .
  • Taborsky , M. , Hudde , B. and Wirtz , P. 1987 . Reproductive behaviour and ecology of Symphodus (Crenilabrus) ocellatus, a European wrasse with four types of male behaviour . Behaviour , 102 : 82 – 118 .
  • Thorpe , J. E. 1986 . “ Age at first maturity in Atlantic salmon, Salmo salar: Freshwater period influences and conflicts with smolting ” . In Salmonid age at maturity , Edited by: Meerburg , D. J. 7 – 14 . Ottawa : Canadian Special Publication of Fisheries and Aquatic Sciences 89 .
  • Thorpe , J. E. 1991 . Acceleration and deceleration effects of hatchery rearing on salmonid development, and their consequences for wild stocks . Aquaculture , 98 : 111 – 118 .
  • Thorpe , J. E. , Metcalfe , N. B. and Huntingford , F. A. 1992 . Behavioural influences on life-history variation in juvenile Atlantic salmon . Salmo salar. Environmental Biology of Fishes , 33 : 331 – 340 .
  • Thorpe , J. E. , Morgan , R. I. G. , Talbot , C. and Miles , M. S. 1983 . Inheritance of developmental rates in Atlantic salmon, Salmo salar L . Aquaculture , 33 : 119 – 128 .
  • van den Berghe , E. P. 1988 . Piracy: A new alternative male reproductive tactic . Nature , 334 : 697 – 698 .
  • Warner , R. R. 1982 . Mating systems, sex change and sexual demography in the rainbow wrasse . Thalassoma lucasanum. Copeia , 3 : 653 – 661 .
  • Warner , R. R. 1984a . Deferred reproduction as a response to sexual selection in a coral reef fish: A test of the life historical consequences . Evolution , 38 : 148 – 162 .
  • Warner , R. R. 1984b . Mating behavior and hermaphroditism in coral reef fishes . American Scientist , 72 : 128 – 136 .
  • Warner , R. R. Alternative mating behaviors in a coral reef fish: A life-history analysis . Proceedings of the Fifth International Coral Reef Congress, Tahiti . pp. 145 – 150 . 4
  • Warner , R. R. 1988 . Traditionality of mating-site preferences in a coral reef fish . Nature , 335 : 719 – 721 .
  • Warner , R. R. and Hofman , S. G. 1980 . Population density and the economics of territorial defense in a coral reef fish . Ecology , 61 : 772 – 780 .
  • Warner , R. R. and Schultz , E. T. 1992 . Sexual selection and male characteristics in the bluehead wrasse, Thalassoma bifasciatum: Mating site acquisition, mating site defense, and female choice . Evolution , 46 : 1421 – 1442 .
  • White , S. A. and Fernald , R. D. 1993 . Gonadotropin-releasing hormone-containing neurons change size with reproductive state in female Haplochromis burtoni . Journal of Neuroscience , 13 : 434 – 441 .
  • White , R. B. and Fernald , R. D. 1998 . Genomic structure and expression sites of three gonadotropin-releasing hormone genes in one species . General and Comparative Endocrinology , 112 : 17 – 25 .
  • White , S. A. , Nguyen , T. and Fernald , R. D. 2002 . Social regulation of gonadotropin-releasing hormone . General Comparative Endocrinology , 112 : 17 – 25 .
  • Winslow , J. T. , Hastings , N. , Carter , C. S. , Harbaugh , C. R. and Insel , T. R. 1993 . A role for central vasopressin in pair bonding in monogamous prairie voles . Nature , 365 : 545 – 548 .
  • Zhou , J.-N. , Hofman , M. A. , Gooren , L. J. G. and Swaab , D. F. 1995 . A sex difference in the human brain and its relation to transsexuality . Nature , 378 : 68 – 70 .
  • Zimmerer , E. J. and Kallman , K. D. 1989 . Genetic basis for alternative reproduction tactics in the pygmy swordtail . Xiphorphorus nigrensis. Evolution , 43 : 1298 – 1307 .

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.