TSD in Reptiles

Modes, mechanisms and

evolution.

Arthur Georges

Applied Ecology Research Group

Sex determination in lizards

Pough et al: Herpetology 1998

Fundamentally Different?

• Genetic sex determination (GSD): Sex determined by genetic factors independent of environment

• Environmental sex determination (ESD/TSD): Sex determined after fertilisation by environmental factors

Outline

• Overview of modes of action of TSD in reptiles

• Dichotomy or Continuum?

• Predisposition for TSD?

• Overview our work, linking to the more specific talk by Tariq Ezaz

TSD

TSD G SD

G SD

Young Georges Doody Canadian J. Zool, in press

Pig-nosed Turtle

1.0C

Georges Stoutjesdijk Limpus J. Experimental Zool. 1994

4.5C

Loggerhead

Water Dragon Harlow 2001, unpubl. thesis

One Pattern?

After Pieau, 1996

Middle Third of Incubation is

InfluentialYoung Georges Doody Canadian J. Zool. in press

Both Magnitude and variability are important

Mean 26C(Male)

Georges Stoutjesdijk Limpus J. Experimental Zool. 1994

Fundamentally Different?

• Remarkable conservatism of vertebrate sexual differentiation genes, including reptiles with TSD.

• Taxonomic distribution of TSD and GSD species suggests both modes have evolved independently multiple times.

~

Evolutionary transitions between the two mechanisms may be relatively simple, perhaps involving one or only a few genes

Sarre Georges Quinn Bioessays 2004

Top Sex Determining Gene

or Gene Complex

WNT4 (?)

DAX1 (?)

WT1 SF1

Aromatasegene

AMH

SOX9

DMRT1

AromataseAndrostenedione

Testosterone

Estrone

Estradiol 17B Receptors

-

-

-

+

++

Sarre Georges Quinn Bioessays 2004

A. Mutually exclusive mechanisms of sex determination

B. Intermediate forms with varying degrees of interaction

A BTSD

TSD G SD

G SD

Dichotomy or Continuum?

Zaborski et al. 1988 Differentiation

Gonad Blood

HY+ HY- HY+ HY-

MALE   100% 50% 50%

H-Y antigen expression(25-26C)

Gonad Blood

HY+ HY- HY+ HY-

FEMALE 100%    50%   50%  

H-Y antigen expression(30-30.5C)

Zaborski et al. 1988 Differentiation

Blood

HY+ HY-

MALE 0 22

FEMALE 42  6 

H-Y antigen expression(at the Pivotal Temp)

Zaborski et al. 1988 Differentiation

Girondot Zaborski et al. 1994 Genetical Research

Blood

HY+ HY-

MALE 3 24

FEMALE 106 7 

H-Y antigen expression(in the field)

Temperature (deg C)

ProportionMALE

Bassianaduperreyi

Shine Elphick Donnellan 2002 Ecology Letters

Temperature Males Females

34 17 47

32 14 14

30 15 15

28 30 26

26 13 17

24 14 10

22 20 15

Bearded Dragon

Present study

Dichotomy or Continuum?

• Extraordinary conservatism in the genes involved in sexual differentiation across vertebrates

• Abundant examples in fish of co-existence of genetic and environmental influences

• Evidence of co-occurrence of genetic and environmental influences in at least some reptiles

• Relative ease by which species appear to have moved from one mode to the other in evolutionary history

Sister TaxaA.muricatus

A.norrisi

Coincidence?

Homeotherms Ectotherms Poikilotherms

Strictly

GSD

TSD

Common

TSD

Rare

Top Sex Determining Gene

or Gene Complex

SexDifferentiation

Genes

Hormonal

Environment

Range of temperatures experienced up to 23C

(22 – 45C)

Top Sex Determining Gene

or Gene Complex

SexDifferentiation

Genes

Hormonal

Environment

Network of genes and gene products

Thermal Compensation

Consistent signal

TSD

Challenging Opportunities for the Future

Reptiles provide tractable opportunities for studying

vertebrate sex determination through the provision of eggs for study before sex is determined, and provision of numerous examples of GSD/TSD models for study.

Viewing GSD and TSD as discrete and fundamentally different processes is overly myopic and distracts us from the possibility that genotypic and environmental influences may interact in determining sexual phenotypes.

Challenging Opportunities for the Future

Comparative approaches, where closely related

species with differing modes of sex determination are selected, show great promise.

Reptiles may well be predisposed to TSD. We aught to be looking for evidence of temperature compensation in the expression of sex genes in GSD species to provide insight into where to look for changes accompanying the move to and from TSD.

The Team

Applied Ecology Research Group Dr Stephen SarreAlex QuinnBrett LidburySean DoodyEnzo Guarino

Comparative Genomics Group

Australian National University

Prof Jenny Graves

Dr Frank Gruetzner

Dr Ann Gaeth

Dr Tariq Ezaz

Funding

ARC Discovery Grants 1996, 2003, 2004-6UC Research Grant 2002CRC for Freshwater Ecology

Collaborators

Hofstra University, USA

Dr Russell Burke

University of Sydney

Prof. Rick Shine

Contributors

Differential Advantage

When environmental conditions favour fitness of one sex over the other, and when information on which sex is to be favoured is not available at the time of nesting, the decision on sex is deferred.

• Temperature during incubation confers differential advantage, directly or indirectly.

• TSD defers the decision until information on the direction of that advantage is available.

Crews: Evolution and Development 2003

Top Sex Determining Gene

or Gene Complex

SexDifferentiation

Genes

Hormonal

Environment

• Networks not “linear” sequences of gene action

• Redundancy in function• Complex system of thermal compensation

Temperature