Transcript Gastrotheca riobambae

Parallel Evolution of Derived Modes
of Reproduction in Amphibians
Marvalee H. Wake
University of California, Berkeley
XI Spanish-Portuguese Herpetological Congress
6-9 October 2010
The Evolution of Viviparity
I study comparative reproductive biology and development, especially
the evolution of live-bearing in frogs, salamanders, and caecilians.
Study of the evolution of viviparity provides the potential for
examination of mechanisms by which the phenomenon arises,
especially the evolution of features that are similar in different
lineages.
Similar traits that have evolved independently in lineages not
associated with derivation from a common ancestral state are
labelled homoplasies.
Homoplasies are often identified (declared) by mapping characters
on a tree representing the phylogenetic relationships of taxa. If
features that appear “the same” occur in distantly related lineages,
they are considered homoplasious.
Because the research goal is often either the phylogeny itself or the
identification of homoplasy, few attempts been made to assess the
mechanistic basis for the evolution of homoplasious conditions.
Kinds of homoplasies
1. Convergence--similar features develop in distantly
related lineages, not derived from a shared ancestral
condition, and via different generative programs.
2. Reversal--features thought lost in lineages recur (genetic
basis is retained and recalled).
3. Parallelism--similar features develop from a common
(identifiable?) substrate/program, elicited independently
in different lineages by the same or different “signals”.
(Less well characterized…)
Do these cases overlap conceptually and pragmatically?
Are they kinds of homology, or is homoplasy conceptually
different?
Why is parallelism important in evolution?
How does live-bearing arise???
1.
I examine both maternal and embryonic properties of live-bearing
development: the condition of the mother (e. g., ovaries, oviducts,
and skin), the trajectory and characteristics of development of
the embryos/fetuses, and ecology and behavior.
2.
I use a diversity of techniques (developmental, morphological,
analytical).
3. I examine several taxa within each of the comparator clades,
rather than a single typological example, in order to assess both
within-clade and across-clade similarity and variation.
4. I use the evidence drawn from my studies to generate hypotheses
about the mechanisms by which the evolution of live-bearing has
occurred.
Viviparity (live-bearing) has arisen many times and in many ways
among amphibian taxa, including:
Males that brood their young in their vocal sacs (Rhinaderma darwini)
or pouches on their legs (Assa spp.);
Females that brood their young in their stomachs (Rheobatrachus
spp. †);
*Intraoviductal retention through late larva or complete
metamorphosis, often with maternal nutrition (some species now †);
*Intraoviductal cannibalism in Salamandra salamandra bernardezi and
S. s. fastuosa (derived recently and independently);
*Back-brooding in frogs. (* = work in my lab, in part)
I will quickly and very briefly show you a few examples, but then
focus on back-brooding in frogs and intraoviductal viviparity in frogs,
salamanders and caecilians as examples of analyses of parallelism-this will be a broad (and brief) overview.
Rheobatrachus silus †
Rheobatrachus
SE Australia silus †; SE Australia
Stomach-brooding
Photo:
Michael Tyler frog
Stomach-brooding frog
Rhinoderma darwini
Patagonia
Photo: Dante Fenolio
Male vocal sac brooder
Assa darlingtoni
Australia
Photo: Unidentified
Male with metamorph
emerging from inguinal
pouch
Eleutherodactylus jasperi †
Puerto Rico
Photo: M. H. Wake
Pregnant female with unborn oviductal froglets (removed)
Nectophrynoides asperginis
East Africa
Photo: Dennis Demello
Ovoviviparous; range size of a football field
Example: Back-brooding through late tadpole or
metamorph in the frogs Gastrotheca
(Amphignathodontidae) and Pipa (Pipidae)
(Research programs of E. del Pino [in particular], R. Jones, W. E.
Duellman, R. Elinson, L. Trueb, M. H. Wake)
Gastrotheca
riobambae
Photo: Luis Coloma
Flectonotus pygmaeus
Mauricio Rivera
Gastrotheca testudinea
Photo: J. Köhler
Gastrotheca fissipes
Photo: Celio Haddad
Gastrotheca guentheri
Photo: Unidentified
Amphignathodontidae
(Hemiphractidae)
43 of 86 species in
the clade.
Wiens et al., 2007.
Evolution 61:18861899.
Gastrotheca riobambae pouch opened, dorsal pouch wall reflected to
expose dorsal and ventral epidermis of the pouch; eggs removed
(Jones et al. 1973)
Gastrotheca testudinea pouch opened and reflected; nearbirth froglet exposed; thin bell gills cover surface
Photos: J. Chin/MHW
B.
C.
po
A.
Gastrotheca riobambae
A. Pouch opening (po) ; B. Eggs on back under skin;
C. Eggs exposed (SVL 36.7 mm; ~ 70 ova, each 3.2 mm dia; two layers)
Gastrotheca longipes
D. Eggs under skin; E. Eggs
exposed (SVL 73. 5 mm; 17
ova, each 11. 5 mm dia)
D.
E.
Photos: J. Chin, D. Buckley, MHW
E.
Pipa arrabali
Photo: Adrian Garda
Pipa parva
Photo: Dante Fenolio
Pipa carvalhoi
Photo: Alex Haas
Pipa stethlageae
Photo: Peter Janzen
Pipa pipa
Photos: Peter Janzen
Close-up of embedded embryos
*
*
*
*
U
*
U
T
T
F
Quic kTime™ and a
dec ompr es sor
are needed to s ee this pic tur e.
T
T
* = Available for this study.
F = Froglets; T = Tadpoles;
U = Unknown
Trueb and Massemin, 2000.
Amph.-Rept. 22:33-54.
A.
Pipa arrabali embryo in pouch
C.
B.
Pipa arrabali pouch skin; note lower layer
D.
Oviduct of a pregnant Pipa arrabali
E.
Ovary with corpus atreticum and ‘mature’
ovum in postovulatory Pipa snethlageae
Oviduct of a postovulatory Pipa snethlageae
Photos: D. Buckley/MHW
Summary of Example:
1.
In both clades, estrogen prepares the dorsal skin for ‘pregnancy’, and
progesterone conditions and maintains gestation. However, the skin
response differs between and even within clades. The oviducts maintain
their responses to the hormones throughout gestation.
2.
Courtship and amplexus differ dramatically between these aquatic and
terrestrial clades; however, in both cases, behavior has evolved so that
females assume postures that allow the males to guide fertilized ova to
their backs.
3.
Embryos develop modifications for respiration/gaseous exchange during
gestation--bell gills in Gastrotheca, expanded, highly vascularized tails in
Pipa.
4.
The mechanism of control of timing of parturition is not known. However,
corpora lutea resorb well before ‘birth’ in G. riobambae, so loss of
progesterone and increase in prolactin may be involved, so duration of
corpora lutea may determine stage of development at birth, probably in
both clades. New data suggest that the length of time the pregnancy can
be maintained determines whether or not metamorphosis will be
completed before birth.
Example: Intraoviductal development to
metamorphosis, with maternal nutrition
following yolk resorbtion, in frogs,
salamanders, and caecilians
(Research programs of F. Xavier, H. Greven, G. Guex, J.-M.
Exbrayat, M. H. Wake)
V Od
V Od
VB
VSt, L
VB
V Od
V VS
V Od
Nectophrynoides viviparus
Photo: David Moyer - WCS
Nimbaphrynoides occidentalis
Photo: Mark-Oliver Rödel
Nimbaphrynoides occidentalis
Photo: Mark-Oliver Rödel
Nectophrynoides tornieri
Photo: M. Menegon
Nectophrynoides asperginis
Photo: Dennis Demello
Oviparity
Ovoviviparity
Viviparity
D. Buckley, unpubl.
lusita
nica
c auca
sica
L ycia
s al am
andr a
Salam
andra
algira
Salam
andra
atra
Salam
andra
corsi
ca
Salam
andra
lanza
i
Salam
andra
se me
novi
Salam
andra
infrai
mmac
Salam
ulata
andra
sa lam
andra
Salam
l ongi
andra
rostri
sa lam
s
a
n
dr a g
Salam
i
g
lioli
andra
sa lam
a
n
dr a b
Salam
e rna r
andra
de z i
sa lam
andra
Salam
alma
andra
nzori
s
sa lam
a
n
dr a c
Salam
re spo
andra
i
sa lam
andra
Salam
more
andra
nic a
sa lam
a
n
dr a s
Salam
alam
andra
andra
sa lam
a
n
dr a e
Salam
urop a
andra
ea
sa lam
andra
Salam
f as t u
andra
osa
sa lam
a
n
dr a g
Salam
allaic
andra
a
sa lam
andra
be jar
ae
siella
lossa
s"
Me rte
n
C hiog
"N ew
t
Salamandra atra
Salamandridae; Wengen, Switzerland
Pregnant female with near-birth fetus (note its
gills, nearly complete limb development, etc.)
*
?
*
*
*
*
*
*
*
*
*
Tree from
Wilkinson and
Nussbaum,
2006
* Indicates that the
genus includes one or
more viviparous species
Viviparous Caecilians
Dermophis mexicanus
Guatemala
Photo: Sean Rovito
Scolecomorphus vittatus
Tanzania
Photo: John Measey
Gymnopis multiplicata
Costa Rica
Photo: Michael Fogden
Chthonerpeton indistinctum
Uruguay
Photographer: Mirco Sole
Dermophis mexicanus Intraoviductal Fetuses
Photo: M. H. Wake
Geotrypetes seraphinii
Ghana
Photo: Dante Fenolio
Chthonerpeton indistinctum
Uruguay
Photo: Mirco Sole
SEM of oviduct of early pregnant D. mexicanus
(Lai and Wake, unpubl.)
Pregnant
Female
Oviductal
Epithelium
Dermophis
mexicanus (Wake,
1980)
Fetal Teeth
(SEM)
Salamandra atra (Greven,
1998)
SEM of pregnant
‘uterus’ of Thamnophis
ordinoides (Blackburn
et al. 2002)
Parallelisms!
SEM of oviduct of Salamandra atra
(Guex and Greven, 1994)
A.
Non-pregnant PAS Hx
D.
Post-pregnant PAS Hx
B.
Mid-pregnant Best’s Carmine
E.
Ovary with maturing ovum
and corpus luteum
C.
Mid- late-pregnant Sudan Black B
Histochemistry of Dermophis mexicanus Oviduct; Ovary
Main Points of this Research:
1.
Both oviducts and skin respond morphologically and physiologically
to ovarian hormones by proliferation, hyperemia, and increased
vascularity. The oviductal morphology is similar across taxa,
although the secretions of the cells vary in composition; i. e.,
morphology can be “the same”, but what it produces biochemically
and physiologically (and behaviorally) can differ considerably
across taxa.
2.
Little is known about hormones and effects in gestation,
development, metamorphosis, and birth; several, especially
prolactin, are ignored.
3.
Embryos/fetuses evolve clade-specific means of facilitating
gaseous exchange, obtaining nutrients, etc.
4.
Maintenance of development in or on the body of a parent is a
complex interaction of morphology, development, endocrinology,
and ecology, as well as historical contingency, that is
underappreciated, understudied and deserving extensive attention.
It is especially important to rectify this, given that the existence
of many species with derived modes of reproduction is threatened.
What, then, is homoplasy; in particular, what is
parallelism??
Is it pattern, process, or the end result--the phenotypic
expression?
Is it a combination of these?
Is it all attributable to “deep homology”?
My analyses suggest that it is indeed “all of these”, and more.
Any attempt to understand homoplasious features requires a
hierarchical analysis of the probable mechanisms that underlie
development and maintenance.
How and why selection operates in the evolution of these
modes has been suggested (the “cold hypothesis”, competition
for resources, reduction of larval predation, etc., etc.), but
not often demonstrated, and never in the full complexity of
the molecular, cellular, organismal, and ecological interactions
involved.
Similarly, homoplasy should not be merely an “end product” or
phenotypic expression.
For example, is “viviparity” in all its forms the same state, or
does the term cover a diversity of processes and “end
products” at several different levels of biological
organization? If so, what components are homologous, and
what are homoplasious?
These are not necessarily new ideas, but I try to frame them in a
more holistic context. Homoplasy, including parallelism, is
demonstrably a major phenomenon in evolution, now more
accessible to study.
1.
Parallelism in particular illustrates both constraints--an
organism can only use the material it has--and opportunities-there are innovative ways to use that material in response to
selection, and they may co-occur in distantly related lineages.
2. The study of the mechanistic basis of homoplasy opens new
ways to explore the selection pressures that elicit responses
that are mechanistically and phenotypically similar.
3. The examination of homoplasious evolution requires a
hierarchical research framework that examines features and
mechanisms at a diversity of levels of organization.
Acknowledgements
I appreciate the invitation from to speak at this most interesting
meeting.
I thank the many colleagues who have provided materials for my
studies of the evolution of live-bearing modes of reproduction in
amphibians, either via collecting or loans from the collections in their
charge.
I appreciate many discussions and collaborations with my students,
postdocs, and colleagues about life history evolution, pattern and
process of evolution, and why amphibians are the most interesting
animals in the world, especially caecilians.
The support of the National Science Foundation, agencies of the
University of California at Berkeley, the John Simon Guggenheim
Memorial Foundation, the American Philosophical Society, the Radcliffe
Institute for Advanced Study, the Smithsonian Tropical Research
Institute, and other groups has made the research possible.
I thank you for your attention.