Neuroendocrine control of

reproduction in teleost fish

Olivier Kah
Oncorhynchus gorbuscha
Photo: JE Randall

Universit de Rennes 1
Rennes, France
O. Kah Montevideo-1 2007

Rennes

O. Kah Montevideo-1 2007

Saint Thgonnec

Plougrescant

Rennes

Mont Saint Michel

Saint Malo

Quiberon

Pointe du raz

Carnac

O. Kah Montevideo-1 2007

Main objective:
Provide an overview, as integrative as
possible, of the molecular and cellular
mechanisms which, at the brain level,
participate in the regulation of successful
reproduction in teleost fish
To provide insights into other satellite aspects:
- Historical aspects (concepts and ideas)
- Mechanisms underlying evolution
- Technical aspects
O. Kah Montevideo-1 2007

Outline
The gonadotrophins
Organization of the hypothalamo-pituitary complex in
fish
Brain factors influencing gonadotrophin release
The steroid feedback
Regulation of sexual behaviour
Integration of the photoperiodic message
Endocrine disrupters
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What are
Teleost fish?
O. Kah Montevideo-1 2007

Charles Robert Darwin

(1809-1882)

http://darwin-online.org.uk/

The Origin of Species (1859)

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Porifera

The metazoa

Cnidaria
Ctenophora
Arthropoda
Onychophora
Tardigrada
Annelida

Ecdysozoa

Pogonophora
Vestimentifera
Echiura
Mollusca
Sipuncula

Lophotrochozoa

Bilateria

Nemertea
Plathelminthes

Chordata
Hemichordata
lophophorates
Chaetognatha

Deuterostomia

Echinodermata
pseudocoelomates
http://phylogeny.arizona.edu/tree/eukaryotes/eukaryotes.html

Placozoa
O. Kah Montevideo-1 2007

Teleost fish
Lampreys

Birds

Mammals

Reptiles
Amphibians

Bony fish

Sharks
and rays

Land
vertebrates

Vertebrates
Prochordates
Cephalochordates
Urochordates
O. Kah Montevideo-1 2007

Teleosts

Tetrapods

25 000 sp.

25 000 sp.
Mammals
Amphibians

Reptiles

Birds

Early teleosts

Amia

Early tetrapods
Gar pike

Sturgeon

Coelacanth
Polypterus
Paddlefish

Crossopterygians
Lungfish

Palaeoniscids

Actinopterygians
Ray finned fish

450 Ms
years

Sarcopterygians
Lobe finned O.fish
Kah Montevideo-1 2007

Fish
(25 000 sp.)

Tetrapods
(25 000 sp.)

Zebrafish
Zebra

Whole-genome duplication?

Biodiversity
Resource
Model

450 000 000 years

VERTEBRATES
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Susumu Ohno
(19282000)

Evolution by Gene Duplication.

Berlin: Springer Verlag 1970.
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Whole genome duplication events in vertebrates

1:2:4 rule
1:2:4:8 rule

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Evolution of the
Hox gene
clusters during
vertebrate
evolution

From Meyer and Mlaga-Trillo, 1999

O. Kah Montevideo-1 2007

Teleosts have undergone a rapid radiation

that is unparalleled in other vertebrate taxa.
Number of
Living species

360

Reptiles

23 550

Amphibians
Lungfishes

Coelacanths

Non-teleosts

44

Lobe-finned fish

Birds

Tetrapods

Mammals
310

>235
Teleosts

Whole-genome duplication?

23 637

Ray-finned fish

450

Venkatesh, 2003
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Evolution of teleost fishes

Teleosts

Actinopterygians
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Based on 42
orthologous
genes from
10 model species

From Steinke et al., 2006

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Fish genomes seem to be plastic in comparison with

other vertebrate genomes because of frequent
genetic changes:
polyploidization
gene duplications
gain of introns
rapid speciation

Venkatesh, 2003
O. Kah Montevideo-1 2007

Coho
25 000 species of fish, but only a few
ofsalmon
them
are studied
Catfish
Very important
variability
in
Eel
Sea bass
Goldfish
- Phylogenetical
Rainbow troutposition
- Biology
- Life cycle
Flatfish
Carp
- Reproductive
strategies
Seabream
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From http://www.digitaldiver.biz/cpg/index.php

Sexual reproduction
is the most
common type of
reproduction in fishes
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Asexual reproduction

Sexual reproduction

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Asexual reproduction
- Simply produce an identical copy of yourself
quick and easy
all members of the species have similar vulnerabilities.
Budding

Fission

Parthenogenesis
Daphnia

parent
bud

Hydra

Planarian
O. Kah Montevideo-1 2007

Sexual reproduction is the most common

form of reproduction in metazoa
Sexual reproduction
consists
in the fusion of
haploid gametes (n)
giving birth to
a diploid zygote (2n)
This fusion results in a new and unique
combination of alleles
This allows increasing the variation on which
natural selection can operate
O. Kah Montevideo-1 2007

Sexual reproduction allows

genetic recombination
beneficial mutations from separate
ancesters can be combined
beneficial mutations can be separated
from deleterous mutations
unsuccessful genetic traits can easily
disappear from an existing population
The Origin of Species (1859)
O. Kah Montevideo-1 2007

Sexual reproduction
is much more complicated

- Different individuals produce

sperm and eggs
- Find of a member of the
opposite sex
- Satisfy the partner's selection
criteria
- Ensure fecondation through
successful mating

O. Kah Montevideo-1 2007

Production of haploid gametes requires

reduction of the number of chromosomes

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Gametogenesis is the
process that permits
formation of gametes
from a small number
of germ cells
Meiosis

Spermatogenesis

Ovogenesis
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The final objective

of sexual reproduction
is fertilization

Fertilization has 3 main functions:

transmission of genes from
parents to progeny
restoration of the 2n number
of chromosomes reduced during
meiosis
initiation of development

O. Kah Montevideo-1 2007

Sexual
reproduction
implies the
existence
of separate sexes
Gonochorism = Hermaphrodism

O. Kah Montevideo-1 2007

In mammals, sex is determined genetically

Sox-9, DMT1?, ?
(17q24)

SRY
(Yp)

WT1
(11p13)

(9p)

(10q)

Z=DSS?

AMH

(Xp21)

(19q13)

TESTIS

SF1
(9q33)

SRY

O. Kah Montevideo-1 2007

Only in two species of teleosts,

O. latipes and O. curvinotus,
is sex genetically-determined by Dmrt1bY
Dmrt1bY is 10 Million years old
and is the youngest male
sex-determining system in vertebrates

From Shartl, 2004

Dmrt1bY= dmy expression in medaka

embryonic testis
O. Kah Montevideo-1 2007

In most teleost fish, sexual differentiation

is strongly influenced by hormonal,
environmental or social factors
that are poorly understood

High plasticity of the phenotypic sex in fish

Farlowella amazonum Photo Johny Jensen

O. Kah Montevideo-1 2007

Although sexual reproduction is the most

common type of reproduction in fishes,
there are cases of asexual reproduction

The Amazon molly

Poecilia formosa

Spermato-dependent
gynogenesis (very
rare):
the role of sperm
(from closely related
species) is just to
activate the ovocyte

All female species

O. Kah Montevideo-1 2007

Teleost fish exhibit a tremendous variety

of reproductive strategies:
Sexuality:
From strict gonochorism to simultaneous
functional hermaphrodism
Orange spotted grouper
(perciform)

Gilthead seabream

Protogynous

Protandrous

hermaphrodite:
From female to male

hermaphrodite:
From male to female

(perciform)

Hypoplectrus unicolor
(perciform)

Simultaneous
hermaphrodite

O. Kah Montevideo-1 2007

Teleost fish exhibit a tremendous variety

of reproductive strategies:
Sexuality: alternative strategies
Mixed mating strategies
Social induction of sex differentiation
Gobiodon erythrospilus
(perciform)

Kryptolebias marmoratus

Hermaphrodites reproduce
by either self-fertilisation or
cross-breeding.

Chooses its sex

according to that of
a potential partner
O. Kah Montevideo-1 2007

Gobiodon erythrospilus, el
campen del mundo
de la plasticidad sexual
Photo: JE Randall

inmaduros

maduros

J+
J+
En la presencia de un adulto,
los inmaduros maduran

El sexo del adulto

determina el sexo
del individuo inmaduro

Hobbs et al., 2004

Induccin social de la maduracin y de la

determinacin sexual
O. Kah Montevideo-1 2007

Teleost fish exhibit a tremendous variety

of reproductive strategies:
Stickleback male
Spawning:
Watching Eggs in Nest.
From collective pelagic
spawning without egg
caring
to sophisticated sexual
behaviours (nest
building) followed by
parental care

O. Kah Montevideo-1 2007

Teleost fish exhibit a tremendous variety

of reproductive strategies:
Parental behaviour:
From no care to mouth incubation

Tilapia
O. Kah Montevideo-1 2007

Teleost fish exhibit a tremendous variety

of reproductive strategies:
Viviparous with internal fertilization

Mosquitofish
Gambusia affinis,
Guppy
Poecilia reticulata
O. Kah Montevideo-1 2007

Reproductive strategies
influence the
number and size
of the eggs
Egg number and size diversity in some teleost fish
Species

Mean fecundity
egg number/kg

Turbot
1 000 000
Cod
500 000
Carp
50 000-100 000
Salmonids
2000-3000
Tilapia (Oreochromis) 50-200
Tilapia (Tilapia)
50-100

Egg diameter

1.02
1.4
1-1.5
4-5.5
2-4
1-2

Particularities

Floating, pelagic
Floating, pelagic
Adhesive (vegetal)
Benthic
Maternal
Substrate breeding

From Jalabert, 2005

O. Kah Montevideo-1 2007

Types of gonadal development

Synchronous: annual spawner
Salmonids

Group-synchronous: several spawning each year

Sparus aurata

Asynchronous: daily spawning

Oryzias latipes

O. Kah Montevideo-1 2007

The success of the reproductive process

implies that:
Gametogenesis occurs nomally
Male and female gametes meet at the
most appropriate period for the
survival of progeny
All this is ensured by
hormonal interactions
along the

brain-pituitary-gonad
axis
O. Kah Montevideo-1 2007

In all vertebrates, the

hypotalamo-pituitary complex
controls gonadal activity

O. Kah Montevideo-1 2007

In all vertebrates, gametogenesis

is controlled bypituitary hormones:
The gonadotrophins

O. Kah Montevideo-1 2007

Gonadotrophin
secretion is
under control of
the brain,
notably the
hypothalamus

O. Kah Montevideo-1 2007

Historical overview

Aristotle (II before Christ): the brain is necessary for the

maintenance of body integrity

Mondino de' Luizzi in Anathomia. Galen of Pergamon (II century) described

the hypothalamic infundibulum and the pituitary gland
XIV century edition
in De Usu Partium as the draining route and receptacle,
respectively, for mucus passing from the brain ventricular
structures to the nasopharynx
Mondino deLuizzi (1316) third ventricle serves
as an "integrator" of body functions
Andreas Vesalius (16th century) published the first
anatomical depiction of the infudibular-pituitary stalk
in De Humani Corporis

Andreas Vesalius: De Humani Corporis (1543)

O. Kah Montevideo-1 2007

Historical overview

Leonardo da Vinci
(1508-1509)

Pituitary

Michelangelo Buonarroti, Creation of Adam

Sixtine Chapel
in the Vatican (1508-1512)

O. Kah Montevideo-1 2007

Historical overview
1664

Willis in his "Cerebri Anatome" argues that humors out of the third
ventricle may be carried to the pituitary gland

1742

Lieutand discovers vessels in the pituitary stalk

1778

Sommering introduces the term "hypophysis"

1860

Von Luska describes the primary (or hypothalamic) capillary

plexus of the portal vessels

1872- 1877

Meynert and Forel define the anatomical borders of what they call
"the neural portion extending forward the region of the
subthalamus" (i.e. the hypothalamus)

1893

His introduces the term "hypothalamus" and provides the first

anatomical subdivision based on ontogenesis of the human
brain

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Camillo Golgi Not only invented the Golgi apparatus

(1843-1926)
Nobel prize 1906

1852-1934
Professor of histology But also the Golgi
silver impregnation
University of Pavia
technique (1873)
the black reaction

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Discovery of the connections between the

brain and the posterior hypophysis

Santiago Ramon y Cajal

(1852-1934)
Nobel prize 1906

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The concept of neurosecretion

Ernst Scharrer (1905-1965)
The Journal of Comparative Neurology
55: 573-576 (1932)

Phoxinus laevis
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Historical overview
1930: Popa and Fieldingdescribe
a portal vascular system interpreted
as a route of the blood upward the
hypothalamus

1940- 1955: Geoffrey Harris

showed that the hypothalamopituitary portal system carries
brain factors to the anterior
pituitary

O. Kah Montevideo-1 2007

LH-RH
or
mGnRH
Roger Guillemin
from sheep hypothalamus
(Amoss et al., 1971)

Andrew V. Schally
from pig hypothalamus
(Matsuo et al., 1971)

pGlu-His-Trp-Ser-Tyr-Gly-Leu-Arg-Pro-GlyNH2

Nobel Prize Winners in 1977

Stimulates
LH and
FSHthe
release

for their discoveries

concerning
peptide
hormone production of the brain

O. Kah Montevideo-1 2007

Rosalyn Yalow

for the development of

radioimmunoassays of peptide
hormones

Nobel prize 1977

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The characterization of the first hypothalamic peptides

has been the cornerstone of the development of a
new discipline

Neuroendocrinology:
The study of the interaction between the
nervous system and the endocrine glands, in
particular the pituitary

gland

O. Kah Montevideo-1 2007