Comparative Vertebrate Reproduction

1. Comparative Vertebrate Reproduction Part II. Sex and Sexual Differentiation

2. Introduction and Overview • Acquiring the Sexual Phenotype • Genetic Basis of Sex Determination • Hormonal Influences on Sexual Differentiation • Environmental Influences • The Sex Ratio • Sex Allocation

3. Acquiring the Sexual Phenotype • Two primary mechanisms Primary Sex Determination - Gonads form and differentiate into testes or ovaries Secondary Sex Determination – Involves the development of extragonal characteristics - Primary Sex Characteristics - Secondary Sex Characteristics

4. Primary Sex Determination Formation of Indifferent Gonad Origin of Primordial Germ Cells - hindgut endoderm as in mammals - various extraembryonic tissues as in lizards, snakes, and birds

5. Gonad Differentiation Organization of the Mammalian Testis

6. Gonad Differentiation Organization of the Mammalian Ovary

7. Comparative Aspects Fish Ovary - guppy

8. Comparative Aspects

9. Secondary Sex Determination Primary Sex Characteristics Differentiation of duct systems

10. Duct system in male snakes

11. Secondary Sex DeterminationPrimary Sex Characteristics Control of urogenital system development in mammals

12. Secondary Sex Determination Primary Sex Characteristics Differentiation of the genital tuberacle in humans

13. Secondary Sex Determination Secondary Sex Characteristics • Modification in body form (changes in allometry) • Sex-specific modifications in body size and proportions • Changes in coloration • Changes in behavior patterns

14. Secondary Sex Determination Secondary Sex Characteristics Examples of vertebrate sexual dimorphism

15. Genetic Basis of Sex Determination • One or Two Specialized Sets of Heteromorphic Chromosomes (i.e., homologous heterosomes = sex chromosomes) • A heterogametic individual has a 50% chance of producing a haploid gamete containing one of the two types of sex chromosomes - In mammals – heterogametic condition (XY) results in a male; XX or XO = females that are homogametic - In most reptiles and birds, females are heterogametic (ZW notation); ZZ/ZO = males that are homogametic (The “O” means one of the heterosomes is absent.)

16. Anomalous Chromosomal Combinations In Humans • XX males have fragments of Y chromosome translocated to either X or to the autosomes • Nondisjunction of sex chromosomes can lead to aneuploids lacking a normal chromosomal complement (e.g., Klinefelter syndrome – XXY) • Aberrant heterosomal combinations (e.g., Turner syndrome – XO; super female – XXX) Expression of a gene on the Y sex chromosome is responsible for genetic sex determination in mammals. The gene (SRY) results in the production of a testis-determining factor (TDF)

17. Genetic Basis for Sex Determination in Vertebrate Lineages • Cyclostomes and elasmobranchs – unclear • Teleosts – either XX/XY or ZZ/ZW system • Amphibians – XY (heterogametic) • Most reptiles – ZZ/ZW system • Birds – ZZ/ZO (ZO genotype being normal for females)

18. Vertebrate sex determination systems. Phylogeny of major vertebrate clades showing the sex determining systems found in members of the respective clade. ‘Multiple’ indicates involvement of more than one pair of chromosomes in sex determination. TSD: temperature-dependent sex determination. (From: Ezaz 2006)

19. Hormonal Influences on Sexual Differentiation • Artificial or environmentally-induced alteration of one or more of the hormonal signals can alter the sexual phenotype expected from a genotype. • Many non-mammalian vertebrates have an enormous susceptibilty to exposure to endocrine disruptors in the environment (e.g., American alligators). These chemicals (e.g., xenoestrogens or estrogen angonists [mimics] = xenobiotics) can have epigenetic influences during embryonic development or during adult life.

20. Environmental Influences* • By eliciting subtle changes in the production, reception, and timing of the hormonal signals involved in sexual differentiation, environmental influences can act as epigenetic factors affecting the acquisition of sexual phenotype *Some scientists have attributed recent sex abnormalities in animals to pollution by these xenoestrogens. In Britain, for instance, male trout produced female proteins; Great Lakes salmon grew enlarged thyroids, and in polluted spots on both U.S. coasts, male gulls were feminized and females developed an extra oviduct. This all reflects the basis for the emerging science of endocrine disruption... "Scientists have theorized that these abnormalities all resulted from exposures to chemicals that mimic or counteract hormones in the body" (New theory suggests sex in danger. The Osteopath. Summer 1995; 1(3):24).

22. Social Factors • Social environment can trigger change in sexual phenotype (i.e., sex reversals) Banded Wrasse, Halichoeres notospilus: Female.  Caught in the surf in December 2007, early morning at Cabo Real, Km. 21, San Jose del Cabo, Baja California Sur, Mexico, on cut squid bait, utilizing a Carolina rig and size 4 Mustad 92553 hook. This species undergoes a sex reversal at midlife with the females becoming males. Description and photo courtesy of John Snow.

23. Temperature-Dependent Sex Determination (cont.) Temperature-dependent sex determination. Aromatase activity levels during the thermosensitive period (TSP) are regulated by the temperature of the environment and control gonadal differentiation. Changes in the environment temperature before and after TSP do not seem to affect sex. Manolakou et al.Reproductive Biology and Endocrinology 2006 4:59 doi:10.1186/1477-7827-4-59

24. The Sex Ratio • Expressed as the relative proportion of male and female phenotypes within a population • Primary sex ratio – Male/female ratio produced at the time of fertilization. • Secondary sex ratio – Ratio following completion of parental investment in the offspring. (can reflect the TSD during development, differential pre-partum mortality, and differential mortality during post-hatching or post-partum parental care. • Tertiary sex ratio (operational sex ratio) – Sex ratio representing the relative number of adult males and females within a population. • Ratio commonly expressed as the number of males divided by the number of females in a given population

25. Sex Allocation • Partitioning of male and female reproductive function among different individuals. Different patterns of sex allocation reflect the specific environmental pressures on a particular lineage • Gonochorism – bisexual phenotypes established early in life and persist throughout adult life. • Hermaphroditism –individuals that are capable of functioning as both a male and a female during the course of their life are said to be hermaphroditic or cosexual.

26. Types of Hermaphroditism • Sequential or serial hermaphroditism – individuals are capable of alternating between the production of male and female gametes over the course of their lives. • Sequential hermaphrodites are commonly undergo sex reversal. If sex reversal occurs more than once during a lifetime, this double sex reversal is known as diandry or biandry. • Simultaneous or synchronous hermaphroditism– produce functional male and female gametes at the same time.

27. The Black Hamlet(Hypoplectrus nigricans) • Having the ability of coordinated alteration of sexual phenotype with each member of a mated pair switching between the process of the production of ova and sperm is termed egg trading. - a special type of sequential hermaphroditism called protogynous herma- phroditism = protogyny (– initially a female) in a species where male size impacts fitness. Black Hamlet

28. The Knobbed Porgy(Calamus nodosus) • Sequential hermaphroditism in which differentiation into males occurs first – protandrous hermaphroditism = protoandry (adaptive when large males are not successful at monopolizing females and when larger females produce more ova than do smaller females) • Occurs among eight families of teleosts

29. Normally, synchronous hermaphrodites are not self-fertilizing. The only known self-fertilizing (selfing) species is the mangrove killifish (Rivulus marmoratus). • Most synchronous hermaphrodites possess an ovotestis containing oogenic as well as spermatogenic tissues.

30. Ovotestis Organization in Sea Bass

31. Induced Hermaphroditism (using drugs) Right lobed gonad of a treated male R. pipiens (0.1 ppb atrazine) with anterior testes and developing posterior ovary. (A) Gonad fixed in Bouin’s solution; white arrows show areas where transverse cross-sections were taken. (B) Anterior portion is testicular, with lobules that contain spermatids; white arrows indicate lobules with spermatids. (C) Posterior portion of the gonad has large testicular oocytes. Bar = 250 μm for (A–C). From Hayes et al. (2003) VOLUME 111 | NUMBER 4 | April 2003 • Environmental Health Perspectives

32. Ovotestis in TrueHermaphrodites in Humans • Case 3. Ovotestis in true hermaphrodite. A, testicular compartment shows solid tubules filled with immature Sertoli cells and germ cells (arrow). B, ovarian compartment has numerous primordial and growing follicles containing primary oocytes within the ovarian cortical stroma. C, primordial follicles are invested by a single layer of flattened follicular cells (arrow), and each contains a primary oocyte True Hermaphroditism and Mixed Gonadal Dysgenesis in Young Children: A Clinicopathologic Study of 10 Cases. Kyu-Rae Kim, Youngmee Kwon, Jae Young Joung, Kun Suk Kim, Alberto G Ayala and Jae Y Ro. Mod Pathol 2002;15(10):1013–1019.

33. Ovotestis in Humans (continued)

34. A form of synchronous hermaphroditism, called acquired hermaphroditism, occurs in the deep-sea ceratioid anglerfish (Edriolychnus schmidti) The male deep-sea anglerfish attaches himself to the female body and fuses to it. The male shares the female’s blood supply and all systems, except his reproductive system, atrophy. --- a unique ‘individual’is formed out of intraspecific parasitism

35. Ambiguous sexual development can produce pseudohermaphrodites Pseudohemaphrodite anatomy of Diamondback watersnake, Nerodia rhombifer (J. Stanley and S. Trauth, unpubl.)