Comparative Vertebrate
Reproduction
Part II. Sex and Sexual
Differentiation
Introduction and Overview






Acquiring the Sexual Phenotype
Genetic Basis of Sex Determination
Hormonal Influences on Sexual Differentiation
Environmental Influences
The Sex Ratio
Sex Allocation
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
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
Gonad Differentiation
Organization of the Mammalian Testis
Gonad Differentiation
Organization of the Mammalian Ovary
Comparative Aspects
Fish Ovary - guppy
Comparative Aspects
Secondary Sex Determination
Primary Sex Characteristics
Differentiation
of duct systems
Duct system in
male snakes
Secondary Sex Determination
Primary Sex Characteristics
Control of urogenital
system development
in mammals
Secondary Sex Determination
Primary Sex Characteristics
Differentiation of the
genital tuberacle
in humans
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
Secondary Sex Determination
Secondary Sex Characteristics
Examples of vertebrate sexual dimorphism
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.)
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)
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)
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)
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.
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).

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.
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
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
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.
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.
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 hermaphroditism = protogyny (– initially
a female) in a species where male
size impacts fitness.
Black Hamlet
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


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.

Ovotestis Organization in Sea Bass
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
Ovotestis in True
Hermaphrodites 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.
Ovotestis in Humans
(continued)

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
Ambiguous sexual development can
produce pseudohermaphrodites
Pseudohemaphrodite anatomy of
Diamondback watersnake,
Nerodia rhombifer (J. Stanley and
S. Trauth, unpubl.)