Hormones and Reproduction of Vertebrates. Amphibians

227 Pages·2010·6.17 MB·English

by  David O. Norris and Kristin H. Lopez (Eds.)

Hormones and Reproduction of Vertebrates, Volume 1dFishes
Hormones and Reproduction of Vertebrates, Volume 2dAmphibians
Hormones and Reproduction of Vertebrates, Volume 3dReptiles
Hormones and Reproduction of Vertebrates, Volume 4dBirds
Hormones and Reproduction of Vertebrates, Volume 5dMammals
Hormones and
Reproduction of Vertebrates
Volume 2: Amphibians
David O. Norris
Department of Integrative Physiology
University of Colorado
Boulder, Colorado
Kristin H. Lopez
Department of Integrative Physiology
University of Colorado
Boulder, Colorado
AMSTERDAM(cid:1)BOSTON(cid:1)HEIDELBERG(cid:1)LONDON(cid:1)NEWYORK
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Dedication
This series of five volumes on the hormones and
reproduction of vertebrates is appropriately dedicated to
ourfriendandcolleagueofmanyyears,ProfessorEmeritus
Richard Evan Jones, who inspired us to undertake this
project. Dick spent his professional life as a truly
comparative reproductive endocrinologist who published
many papers on hormones and reproduction in fishes,
amphibians,reptiles,birds,andmammals.Additionally,he
published a number of important books including The
Ovary (Jones, 1975, Plenum Press), Hormones and
Reproduction in Fishes, Amphibians, and Reptiles (Norris
and Jones, 1987, Plenum Press), and a textbook, Human
Reproductive Biology (Jones & Lopez, 3rd edition 2006,
Academic Press). Throughout his productive career he
consistently stressed the importance of an evolutionary
perspectivetounderstandingreproductionandreproductive
endocrinology. His enthusiasm for these subjects inspired
allwithwhomheinteracted,especiallythemanygraduate
studentshefostered,includinganumberofthosewhohave
Richard Evan Jones
contributedto thesevolumes.
v
Preface
Hormones and Reproduction of Vertebrates Preface to the Series
Every aspect of our physiology and behavior is either Chemical pollution and climate change pose serious
regulated directly by hormones or modified by their challenges to the conservation and reproductive health of
actions,asexemplifiedbytheessentialanddiverserolesof wildlifepopulationsandhumansinthetwenty-firstcentury,
hormones in reproductive processes. Central to the evolu- andtheseissuesmustbepartofourmodernperspectiveon
tionary success of all vertebrates are the regulatory chem- reproduction.Consequently,wehaveincludedchaptersthat
icals secreted by cells that control sexual determination, specifically deal with the accumulation of endocrine-
sexual differentiation, sexual maturation, reproductive disrupting chemicals (EDCs) in the environment at very
physiology,andreproductivebehavior.Tounderstandthese lowconcentrationsthatmimicorblockthecriticalfunctions
processesandtheirevolutioninvertebrates,itisnecessary ofourreproductivehormones.Manyauthorsthroughoutthe
to employ an integrated approach that combines our series also have provided information connecting repro-
knowledge of endocrine systems, genetics and evolution, ductiveendocrinologytospeciesconservation.
and environmental factors in a comparative manner. In Theseriesconsistsoffivevolumes,eachofwhichdeals
addition to providing insight into the evolution and physi- withamajortraditionalgroupingofvertebrates:involume
ology of vertebrates, the study of comparative vertebrate order, fishes, amphibians, reptiles, birds, and mammals.
reproduction has had a considerable impact on the Each volume is organized in a similar manner so that
biomedical sciences and has provided a useful array of themes can be easily followed across volumes. Termi-
model systems for investigations that are of fundamental nology and abbreviations have been standardized by the
importancetohumanhealth.Thepurposeofthisserieson editors to reflect the more common usage by scientists
the hormones and reproduction of vertebrates is to bring working with this diverse assembly of organisms we
together our current knowledge of comparative reproduc- identify as vertebrates. Additionally, we have provided
tiveendocrinologyinoneplaceasaresourceforscientists indices that allow readers to locate terms of interest,
involved in reproductive endocrinology and for students chemicalsofinterest,andparticularspecies.Aglossaryof
who are just becominginterested inthis field. abbreviationsused isprovidedwith each chapter.
Inthisseriesoffivevolumes,wehaveselectedauthors Finally, we must thank the many contributors to this
with broad perspectives on reproductive endocrinology workfortheirwillingnesstosharetheirexpertise,fortheir
from a dozen countries. These authors are especially timely and thoughtful submissions, and for their patience
knowledgeable in their specific areas of interest and are with our interventions and requests for revisions. Their
familiar with both the historical aspects of their fields and chapters cite the work of innumerable reproductive biolo-
thecuttingedgeoftoday’sresearch.Wehaveintentionally gists and endocrinologists whose efforts have contributed
included many younger scientists in an effort to bring in to this rich and rewarding literature. And, of course, our
freshviewpoints.Topicsineachvolumeincludesexdeter- special thanks go to our editor, Patricia Gonzalez of
mination,neuroendocrineregulationofthehypothalamuse Academic Press, for her help with keeping us all on track
pituitaryegonadal (HPG) axis, separate discussions of and overseeing the incorporation of these valuable contri-
testicular and ovarian functions and control, stress and butionsinto thework.
reproductive function, hormones and reproductive behav-
iors,andcomparisonsofreproductivepatterns.Emphasison David O. Norris
the use ofmodelspecies isbalanced throughout the series
withcomparativetreatmentsofreproductivecyclesinmajor Kristin H. Lopez
taxa.
xiii
Preface
Preface to Volume 2 Amphibians
Thisvolumeprovidesabackgroundinthedevelopmentand importanceanditsrolesinthediversereproductivemodes
function of the reproductive system of amphibian verte- exhibited by this vertebrate group. The interaction of the
brates with an emphasis on the roles of bioregulators hypothalamusepituitaryeadrenal(HPA)axiswiththeHPG
(hormones,pheromones,etc.)indirectingtheformationand axisisexploredintheimpactsofstressonreproduction.The
activities of the hypothalamusepituitaryegonadal (HPG) roleofhormonesandpheromonesinreproductivebehavior
axis. Where possible, the topics have been arranged simi- isanotherspecialfocus.Thefunctionsofhormonesaswell
larly to the other volumes in this series to facilitate the asenvironmentalcuesinreproductivecyclesaredescribed
efforts of readers looking for comparative data on repro- for the major amphibian groups (Anura: frogs and toads;
ductiveprocesses. A discussion of the diversityof mecha- Urodela: newts and salamanders; Gymnophiona: caeci-
nismsinvolvedinamphibiansexdifferentiationisfollowed lians).Finally,thereisachapterdealingwiththeimpactsof
by chapters describing the morphology, physiology, and environmental chemicals that function as endocrine dis-
hormonal regulation of the gonads and sex accessory ruptorsofreproductioninamphibians,whichshouldbeof
structures. Maternal adaptation has been selected as a interesttoconservationists,ecologists,andtoxicologistsas
special topic for amphibians due to its evolutionary wellasreproductivephysiologists.
xv
Contributors
Ste´phane Flament, Dominique Chardard, James A. Carr, TexasTechUniversity,Lubbock,TX,USA
Amand Chesnel, and He´le`ne Dumond, Nancy-Universite´, Hartmut Greven, Heinrich-Heine-Universita¨tDu¨sseldorf,
Universite´ HenriPoincare´,Vandoeuvre-le`s-Nancy,France
Du¨sseldorf,Germany
Pei-San Tsai, UniversityofColoradoatBoulder,Boulder,CO,USA Sarah K. Woodley, DuquesneUniversity,Pittsburgh,PA,USA
Catherine R. Propper, NorthernArizonaUniversity,Flagstaff, Rakesh K. Rastogi, Gianluca Polese, and
AZ,USA Biagio D’Aniello, UniversityofNaplesFedericoII,Napoli,Italy
Mari Carmen Uribe Aranza´bal, UniversidadNacional Claudia Pinelli, and Gabriella Chieffi-Baccari, Second
Auto(cid:1)nomadeMe´xico,CiudaddeMe´xico,Mexico
UniversityofNaples,Caserta,Italy
David M. Sever, SoutheasternLouisianaUniversity,Hammond, David O. Norris, UniversityofColoradoatBoulder,Boulder,
LA,USA
CO,USA
Nancy L. Staub, GonzagaUniversity,Spokane,WA,USA
xvii
Chapter 1
Sex Determination and Sexual
Differentiation in Amphibians
Ste´phane Flament, Dominique Chardard, Amand Chesnel, and He´le`ne Dumond
Nancy-Universite´,Universite´HenriPoincare´,Vandoeuvre-le`s-Nancy,France
a terrestrial stage at some point in life. Although a few
SUMMARY
species are viviparous, most species produce eggs
We review here sex determination and differentiation in
surrounded by jelly layers that are deposited in water.
amphibians. Many of the observations and experimental results
Larvae hatch from these protective translucent envelopes
areavailableforboththeAnuraandCaudataorderswhereasthe
literature is very poor regarding Gymnophiona. We describe and,afteraperiodofaquaticlife,theymetamorphoseinto
genetic sex determination that is associated with sex chromo- terrestrial semi-aquatic adults. Some species are neotenic:
somes that display various patterns, from homomorphism to they do not metamorphose or do so incompletely, they
heteromorphism. Gonadal differentiation is also discussed. The retain larval characteristics into adulthood, and reproduce
generalfeaturesleadingtheundifferentiatedgonadtodifferentiate in alarval orsemi-larval state.
asanovaryoratestisappeartobesimilarinanuransandcaudates, Duetotheirdevelopmentbeingrealizedautonomously
but the origin of germ cells is very different. We also focus on
in water, amphibians have been used extensively to study
sensitivitytotemperature,afactorthatcaninducesexreversalin
developmental biology, with the well-known African
several species by modulating steroid hormone synthesis. These
clawed frog Xenopus laevis as an experimental model.
molecules are indeed major players in the sex differentiation
The present chapter reviews recent data concerning an
process.Therecentdiscoveryofasex-determininggene(DM-W)
important event occurring during development: sex
in Xenopus laevis could increase our knowledge of the sex
determination/differentiationprocessinthenearfuture. determination and differentiation. We focus on the sensi-
tivity of these processes to environmental factors, espe-
cially temperature, a factor that can induce sex reversal.
Finally, we describe the effects of steroid hormones that
appear as major players, as well as the genes involved in
1. INTRODUCTION
these mechanisms.
The class Amphibia is comprised of three orders: Anura
(Salientia),Caudata(Urodela),andGymnophiona(Apoda).
2. SEX DETERMINATION
The order Anura (more than 4500 species) includes
frogsandtoadsgroupedintoapproximatelythirtyfamilies, In amphibians, sexcan begeneticallydetermined. Among
of which Leptodactylidae, Hylidae, and Ranidae are the species using genetic sex determination, some are
largest.Salamanders,newts,sirens,amphiuma,waterdogs, male heterogametic (the male is heterozygous at a sex-
andmudpuppiescomprisetheorderCaudata.Thereareten determininglocus)whileothersarefemale heterogametic.
living families grouped into three suborders: Crypto- Some species have reinforced this allelic difference by
branchoidea, Salamandroidea, and Sirenoidea. The largest differentiating sex chromosomes. However, only approxi-
familyisthePlethodontidae(lunglesssalamanders),found mately 4% of the amphibians karyotyped have cytologi-
almostexclusivelyintheAmericas,whichcomprisesmore cally differentiated sex chromosomes (Hillis & Green,
than half of all known caudates (500 species). The order 1990;Hayes,1998;Schmid&Steinlein,2001).Indeed,in
Gymnophionaistheleaststudiedandconsistsofcaecilians most cases, sexchromosomes are homomorphic; i.e., they
that resemble giant earthworms rather than typical are morphologically undifferentiated when studied with
amphibians. classical cytogenetic methods. Hence, the identification of
Althoughthereareseveralexceptions,mostamphibians the heterogametic sex is often deduced from other
are biphasic: they go through an aquatic stage and approaches.
HormonesandReproductionofVertebrates,Volume2eAmphibians 1
Copyright(cid:1)2011ElsevierInc.Allrightsreserved.
2 Hormones andReproduction ofVertebrates
2.1. Sex Chromosomes In other amphibians such as the urodele Pleurodeles
waltl (Gallien, 1951) or the anuran X. laevis (Chang &
Embryonic gonad transplantations were used in classical
Witchi,1955),sexreversalwasobtainedbytreatinglarvae
experiments on the American salamanders Ambystoma
with estradiol (E ). The larvae developed as functional
2
mexicanumandAmbystomatigrinum(Humphrey,1942).In
females whatever their sexual genotype. Half of them,
tail-bud embryos, the primordium of the ovary from one
when crossed with normal males, produced all-male
sideofthebodywasreplacedbytheprimordiumofatestis
progenies, demonstrating female heterogamety (ZW)
takenfromageneticallymaleembryo.Becauseatthisearly
(Figure 1.1(b)).
stage the sex of the individual cannot be recognized, the
Breeding experiments and analysis of the progeny of
right combination occurred in 25% of transplantations.
sex-reversed females have shown a male heterogamety
During the further development of the embryo, the trans-
(XY) in some species (e.g., Rana japonica, Rana rugosa,
planted testis hormonally modified the ovary into a func-
Hyla arborea japonica, Bombina orientalis) (Schmid &
tional testis. As soon as sex reversal was achieved, the
Steinlein, 2001)(Figure 1.1(c)).
transplanted testis was removed. Thus, the sex-reversed
The microscopic observation of lampbrush chromo-
female possessed a testis producing spermatozoa from
somes from prophase I-arrested oocytes could be used to
genetically female germ cells. At adulthood, when these
confirmthepresenceofZZ/ZWsexchromosomes(bivalent
sex-reversed animals were mated with normal females,
IV)in P. waltl (Lacroix,1968a; 1968b). In thatspecies,at
their progeny contained 25% males. This result indicates
ambient temperature, heteromorphic loops in the ZW
thattheAmbystomafemale istheheterogameticsex(ZW)
bivalentarenotvisibleunderaphasecontrastmicroscope,
(Figure 1.1(a)).
but are revealed by in-situ protein immunodetection with
antibodies (Lacroix et al., 1985) orin-situ hybridization
with RNAprobes (Penrad-Mobayed, Moreau, &Angelier,
1998).TheseheteromorphicRNA-labeledloopsconstitute
a specific marker of the differential segment of the sex
chromosomes. The RNA sequence interacts with lamp-
brush loop-associated proteins. This interaction is ther-
mosensitive: treatment of adult animals for 18 hours at
(cid:1)
34 C reduces the labeling signals, whereas treatment for
(cid:1)
seven days at 8 C enhances the labeling signals. The
identity of these sex-specific RNA-bindingproteins isstill
unknown. Using such induced loops as markers, one
trisomic female for bivalent IV (ZZW) was identified,
confirming the major role of the W chromosome in the
mechanism of female sex determination in this species
(Lacroixet al., 1990).
AsimilarsituationwasdescribedinPleurodelespoireti;
atambienttemperature,theWchromosomeofthebivalent
IVhasalsobeendistinguishedbyasetoflampbrushloops
displaying distinct morphology under a phase contrast
microscope (Lacroix,1970).
TheEuropeantreefrogHylaarboreahashomomorphic
sex chromosomes, but male heterogamety was recently
revealedbythesex-specificpatternofamicrosatellite-like
marker(Berset-Brandly,Jaquiery,&Perrin,2006).Atlocus
Ha5-22, all females investigated were homozygous for
allele235andallmaleswere heterozygousforalleles235
and241,pointingtoalocationwithinthenon-recombining
region of nascent sex chromosomes, with allele 235 fixed
FIGURE 1.1 Theoretical percentages of genotypes in progenies from ontheprotoXandallele241ontheprotoY.Thesuccessful
crosses between standard and sex-reversed individuals. (a) In case of amplificationofHa5-22inseveralhylidspeciesaswellas
female heterogamety, with female to male sex reversal obtained after thenatureofitstandemrepeatsuggestedalocationwithin
masculinization of host gonad with testis graft. (b) In case of female
the coding region of a conserved gene. It was recently
heterogamety, with male to female sex reversal obtained after estrogen
identified as the homolog of Med15, a key component
treatment. (c) In case of male heterogamety, with female to male sex
reversalobtainedafterandrogentreatment. of the mediator coactivator complex (Niculita-Hirzel,
Chapter | 1 SexDetermination andSexual Differentiationin Amphibians 3
Sto¨ck,&Perrin,2008).TheXandYallelesdifferbythree heterochromatin. In contrast, the Y chromosome of the
frame-preservingindels(eightaminoacidsintotal)within South American marsupial frog Gastrotheca riobambae is
theirglutamine-richcentralpart.Thesedifferenceshavethe larger than the X; this is a very rare situation among
potential to affect the conformation of the mediator vertebrates (Schmid, Haaf, Giele,& Sims, 1983).
complexandtoactivategenesinasex-specificway.Thus, Amphibians provide a unique example of population
theymightrepresentthefirststepstowardtheacquisitionof variation in male and female heterogamety: the Japanese
amale-specific function. frogR.rugosa(Miura,2008).TheJapanesepopulationsof
The cell membrane-associated HYantigen or a cross- thisspeciesaredividedintofourgeneticformsthatinhabit
reactive antigen is present in the gonad of the heteroga- four different geographical regions. These forms differ in
metic sex (XY or ZW) in all vertebrates so far studied, heterogametic sex determination and sex chromosome
including amphibians. It was used to determine the content. The central Japan form has differentiated XY sex
heterogameticsexinseveralspecieswithhomomorphicsex chromosomes,thenorthwestJapanformhasdifferentiated
chromosomes,includingX.laevis,Bufobufo,Pyxicephalus ZW chromosomes, and the two other forms (Kanto and
adspersus, Rana ridibunda, Pelodytes punctatus, P. waltl, west Japan) display male heterogamety (as deduced from
A. mexicanum, and Triturus vulgaris (for reviews see hormonally induced sex reversal and breeding experi-
Schmid & Steinlein, 2001; Eggert, 2004). ments) but they have homomorphic chromosomes.
Incorporation of the thymidine analog bromodeoxyur- Recently, populations located west of the XY form were
idineintothereplicationbandingwasusedintheEuropean shown to display female heterogamety (Ogata, Ohtani,
waterfrogRanaesculentatoidentifytheXYchromosomes Hasegawa, & Miura, 2008). Since they belong genetically
(pair number four) that are still in a primitive stage of to the XY form, their origin is probably very recent and
morphologicaldifferentiation(Schempp&Schmid,1981). theywere designated asthe Neo-ZW form.
MaleshavealatereplicatingbandinthelongarmoftheY Finally, some amphibians display exceptional types of
chromosomethatislackingintheX.Ithasbeenproposed sex chromosomes. In an endemic New Zealand frog,
that this late replicating band consists of repetitive DNA Leiopelma hochstetteri, a Z chromosome is absent from
since its replicationbeginslater than other regions. bothmalesandfemalesandaunivalentWchromosomeis
Insomecases,sexchromosomescanonlybeidentified present only in females: males are OO (2n ¼ 22) and
byspecificstainingoftheirheterochromatin.Forinstance, females are OW (2n ¼ 22 þ W) (Green, 1988). This W
heterochromatic telomeres are present in the long arms chromosomeisneitherafragmentofanotherchromosome
of only one of the homologs (Y) of the pair number four nor amember ofa multiple ZW1W2/ZZ system.
in Triturus alpestris and T. vulgaris (Schmid, Olert, & In a population of the neotropical frog Eleuther-
Klett, 1979). The mitotic karyotypes of Triturus cristatus odactylusmaussi(leaflitterfrog)fromnorthernVenezuela,
carnifex and Triturus cristatus cristatus are very similar homomorphicXYchromosomesandaderivedY-autosome
and display distinct sex chromosomes (fourth pair). Both translocationcoexist(Schmidetal.,2002).Indeed,females
the X and Y chromosomes are submetacentric. The X have 2n ¼ 36 chromosomes (16 pairs þ XXAA) whereas
chromosome carries a faint C-band in the middle of the 95% of males have 2n ¼ 35 due to a centric fusion (Rob-
short arm and a subterminal C-band on the long arm. The ertsonian)betweenYandanautosome(16pairsþXAAy).
YchromosomecarriesthesetwoC-bandsandanadditional The remaining males (5%) exhibit the same 2n ¼ 36
one on the long arm. chromosomes asdo all the female specimens. Theyrepre-
In other salamanders of the genus Hydromantes, the X sent the ancestral status (XYAA) before the Y-autosome
chromosome is acrocentric while the Yis submetacentric. fusion.
In the X chromosome, heterochromatin is present in the Thus, in amphibians, both male and female hetero-
longarmandatthecentromericregion,whereasintheYit gamety are represented, often in the same family, genus,
is found in the centromeric region and in the short arm species, or even population. However, sex chromosomes
(Nardi, Andronico,De Lucchini, &Batistoni, 1986). arenotoftenevidentlyheteromorphicandspecialsituations
Highly heteromorphic sexchromosomes are present in or methods mustbe used toidentifysexualgenotype.
someamphibians.ThefirstexamplewasfoundintheSouth
AfricanbullfrogP.adspersus(Schmid,1980).Femalesare
2.2. Evolution of Sex Chromosomes
heterogameticandtheWchromosomeissmallerthantheZ
and its short arm is completely heterochromatic. The The best-studied vertebrate sex chromosomes are the XY
AmericansalamandersofthegenusNecturushavethemost system of mammals and the ZW systems of birds and
highly differentiated XY chromosomes yet discovered in snakes(Ezaz,Stiglec,Veyrunes,&MarshallGraves,2006).
the caudate amphibians (Sessions & Wiley, 1985). The Y Inthegeneralcontextofgeneticsexdetermination,agene
chromosomes are about one quarter the size of the X should be at the top of a sex-determining cascade. This
chromosomes and almost completely constituted of master sex-determining gene is generallythought to be an