Download Amphibian Reproduction

Amphibian Reproduction
Ch 8: Reproduction and life histories
Ch 14: Mating systems and sexual selection
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European Common Frog (Rana temporari
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Mexican Tree Frogs (Smilisca baudinii), Belize
Wood Frogs (Lithobates sylvaticus) at Heiberg Forest, Tully 4NY
Outline
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Reproduction in:
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Caecilians
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Salamanders
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Anurans
Heterochrony/Neoteny
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Reproductive strategies: caecilians
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All have internal fertilization
via phallodeum
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Reproductive strategies: caecilians
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Viviparous caecilians retain eggs until the young have developed
– feed on yolk and maternal secretions in the oviducts (watch
video)
Oviparous caecilians lay eggs on land near water and can have an
aquatic larval stage or hatch as small versions of the adult form
(direct development)
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Parental care: caecilians
Dermatophagy: young feed on mother’s enriched
skin cells (Video)
Kupfer et al. (2006) Parental investment by skin feeding in a caecilian amphibian. Nature 440:926-929.
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Reproductive modes: salamanders
Internal vs. External Fertilization
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External fertilization ~ eggs and larvae aquatic
ancestral condition (e.g. Sirenidae, Cryptobranchidae,
Hynobiidae)
• Female hellbenders lay 200-500 eggs in
an aquatic nest made by the male under a
large rock.
• Male fertilizes the eggs after oviposition
by the female.
• Male guards the nest until the young
hatch (2 - 3 months).
• Larval period can be up to 1.5 years.
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Reproductive modes: salamanders
Internal fertilization ~ 90%
of salamander species
 Most salamanders produce
"spermatophores" – sometimes
80-100 per male per season
 Intense courtship as males attempt to convince a
female to pick up their sperm packet
 Females pick these up with lips of cloaca
 Which sex invests more in reproduction is not clear!
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Collective mass of a male’s spermatophores = 1 egg mass
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Spermatophores
deposited by
Ambystoma
maculatum
Patterns of spermatophore deposition by the
spotted salamander (Ambystoma maculatum)
See: courtship video
Sexual interference
by male tiger
salamanders
(Ambystoma
tigrinum)
Reproduction: salamanders
Pheromones ~ increase female receptivity
• “Scratching” pheromone delivery by
Eurycea bislineata
• Protruding premaxillary teeth are visible
just in front of the pad of the mental gland.
• During scratching the male swabs the
female’s surface with this mental gland
(releasing pheromone)
• Then abrades the site with premaxillary
teeth, introducing the pheromone.
•“Vaccination delivery”
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Video
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Plethodon yonahlossee
Plethodon shermani
Click here to learn more about pheromone evolution at
Oregon State University, including courtship and
spermatophore pick-up videos
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Secondary sexual characteristics
Video
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Sperm storage
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Accomplished by females in specialized tubules
(generally the spermatheca)
Leads to the possibility of sperm competition and
multiple paternity of offspring
Also great flexibility in terms
of female mate choice
Greater sexual selection
may lead to evolution of
courtship, e.g. spotted
salamanders
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7 spotted salamander clutches
from near Ithaca
Genotyped all offspring
using microsatellite DNA
Determined that two to eight
males contributed to clutches
Multiple paternity is a common strategy in this
explosively breeding species
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Oviposition sites: aquatic
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Notophthalmus viridescens
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Egg symbioses
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Local phenomenon
involving a unicellular
green alga (Oophila
amblystomatis)
associated with
ambystomatid eggs
Found in stagnant water
and soils
Extremely abundant in
inner envelope of eggs and
gives egg masses a green
hue
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Elements of the symbiosis
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Algae produces
O2
Algae consume
CO2 and N-rich
waste produced
by developing
embryo
↑ fitness
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Protection
against bacteria
Faster
development
Gilbert(1944)
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“Solar salamanders”?!?!
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Photosynthetic algae have been
found inside the cells of larvae
(novel in a vertebrate)
Tagged within embryo cells (A.,
right)
Passed from mother to embryo?
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In oviducts
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Can’t be cultured
Also colonized from water
Links:
Popular press article
Kerney et al. (2011) Intracellular invasion
of green algae in a salamander host.
Proceedings of the National Academy of
Sciences 108:6497-6502.
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Other aquatic oviposition sites –
moving waters
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Salamander eggs laid in water
(reproductive modes I versus II)
Non-aquatic eggs
Bolitoglossa pesrubra
Ambystoma opacum
arboreal
terrestrial
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Reproductive modes: salamanders
Ovoviviparous (10 spp.)
Viviparous
(only Salamandra atra)
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Salamander parental care
Limited to egg guarding
1.
2.
3.
Eastern Newt
(Notophthalmus
viridescens) wraps eggs in
submerged vegetation
Tiger Salamander
(Ambystoma tigrinum)
guards aquatic egg mass
Appalachian Woodland
Salamander (Plethodon
jordani) coiled around
terrestrial eggs
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Eastern Red-backed Salamander (Plethodon cinereus) female with eggs
Kleptogenesis: “Jeff Complex” locally
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Original
hybridization likely
occurring 2.4-3.9
million years ago
Oldest known
lineage of all-female
vertebrates.
The hybridization
was most probably
with an A.laterale.
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mtDNA
All known
unisexuals have at
least one A. laterale
genome
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LLLJ
22 distinct unisexual
Ambystoma with
chromosome numbers
varying from diploid (2 sets)
to pentaploid (5 sets)
LJJJ
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Reproduction without fertilization!
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Unisexual, all-female triploid species in which eggs develop
directly without fusion of egg and sperm via kleptogenesis
JJ
Jefferson’s Salamander
(Ambystoma jeffersonianum)
LJJ
Silvery Salamander
(Ambystoma platineum)
LL
Blue-spotted Salamander
(Ambystoma laterale)
LLJ
Tremblay’s Salamander
(Ambystoma tremblayi)
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To here – post-break
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Northeast Herpetology Workshop 2017
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Dates: June 12-23, 2017 (weekend attendance is optional)
Contact: [email protected]
More Information: http://www.montclair.edu/csam/school-of-conservation/summerworkshops/herpetology/
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Location: New Jersey School of Conservation (NJSOC) in Stokes State Forest, Sussex County, New Jersey
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Description: This workshop is an introduction to the reptiles and amphibians of the Northeast United States and
the techniques that are used to conserve and study them in the field. Through numerous field activities,
participants will acquire vital research skills and hands-on experience with the salamanders, frogs, toads, turtles,
lizards, and snakes that call the Northeast home. A small number of classroom lectures and active learning
discussions will also contribute to the learning experience.
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The workshop includes:
Discussions of reptile and amphibian natural history: their basic biology, life histories, and habitats Discussions on
the conservation and management of reptiles and amphibians Discussions concerning study design Reptile and
amphibian identification and taxonomy Identification of calling amphibians by ear Habitat, plant, and non-herp
animal identification Reptile and amphibian sampling, trapping, and marking/tagging techniques Radiotelemetry
Reptile and amphibian tissue sampling for DNA analysis Collection of occupancy, relative abundance, markrecapture, physical, environmental, and geographic data Field note recordation and organization A primer in
nature photography Day and night surveys for reptiles and amphibians Hikes through several diverse northeastern
habitats Off-site field trips to the New Jersey Pine Barrens and urban habitats near NYC Participation in ongoing
herpetological studies at the NJSOC and elsewhere Meals and lodging at the NJSOC
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Qualifications: No experience is necessary but participants should be capable of college-level work and have
strong interests in field biology, ecology, natural history, etc. Participants should also be in relatively good health
and capable of hiking several miles in a range of conditions over moderate- difficult terrain.
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Cost: The workshop will be divided into two one-week sessions, with each week-long session involving different
Monitoring for Amphibians and Reptiles
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Monitoring for Amphibians and Reptiles by JJ Apodaca, Co-chair of
Partners in Amphibian and Reptile Conservation's Joint National Steering
Committee, and Professor of Conservation Biology at Warren Wilson
College in Asheville, NC
Hosted by Wildlife Habitat Council
Register here: http://www.wildlifehc.org/knowledge-resource/monitoring-forreptiles-and-amphibians/
Date: March 22, 2017
Time: 1 pm to 2 pm EST
You’ll learn:
(1) Active and passive sampling techniques including using surveys and
artificial cover objects
(2) How to collect scientifically rigorous data
(3) Different monitoring techniques for specific taxa
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Amphibian Reproduction
Ch 8: Reproduction and life histories
Ch 14: Mating systems and sexual selection
Continued…
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Caudates
(complete)
Caecilians
(complete)
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Reproductive modes: anurans
Ancestral Mode
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In contrast to salamanders and caecilians,
nearly all anurans have external fertilization
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External fertilization
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Oviposition and external fertilization
by anurans
Prolonged vs. explosive breeders
Associated with permanent habitats
and social systems predicated on
female choice. Examples include
Green Frogs and Bullfrogs.
Associated with ephemeral habitats
and species whose reproduction is
strongly cued by environmental stimuli.
Males may emit release calls when
amplexed by another male. Examples
include Wood Frogs and Spadefoots.
Wells, K.D. (1977) The social behavior of anuran amphibians. Anim.Behav. 25: 666-693.
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Prolonged = resource defense systems: Territorial male
American bullfrog (Rana catesbeiana)
Relationship of male body size to two components of
reproductive success among American bullfrogs (Rana
catesbeiana)
Prolonged = resource defense systems: Territorial male
American bullfrog (Rana catesbeiana) with two satellite
males
Resource defense: Reproductive behavior
of the green frog (Rana clamitans)
Scramble competition: Mating behavior of
the American toad (Anaxyrus americanus)
Thermal dimensions: “communal
dumping”
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Wood frog eggs act like
lenses
Concentrate sun’s rays and
increase egg temperatures
3-5 degrees C above
surrounding water.
Cumulative effect
substantially accelerates
development
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Convection current
through the egg
mass of a wood
frog (Rana
sylvatica)
- promotes tiny
water currents
through the eggs
masses, increasing
the availability of
oxygen to
developing
embryos
Multiple amplexus in the Australian
myobatrachid frog Crinia georgiana
Costa Rican Red-eyed Tree Frogs
Africa Reed Frogs
Amplexus
Common Toads
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Anuran amplexus
Axillary
Cephalic
♀ ♂
Glued
Cloacal
apposition
Inguinal
Straddle
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inguinal
amplexus
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axillary amplexus
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Secondary sexual characteristics
Changes in coloration
Nuptial pad
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Keratinized
“claws” on
hands of male
Leptodactylus
melanonotus
Keratinized spines on chest and
digits of male Paa spinosa
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Reproductive modes: anurans
Incredibly diverse!!! Especially in the tropics
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Trend towards terrestriality
Thought to be driven by lower rates
of predation in smaller bodies of water
and out of water
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Figure 8.18 Some frogs brood eggs
outside the female reproductive tract
Reproductive modes: anurans
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Foam nests
Overhanging water ~ Chiromantis
In water ~ Leptodactylus insularum
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Group spawning by the African gray treefrog (Chiromantis xerampelina)
Reproductive modes: anurans
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On leaves over water
Red-eyed tree frog ~
Agalychnis callidryas
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Reproductive modes: anurans
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Parental care - Female dorsal pouch
Gastrotheca spp.
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“Marsupial” frogs
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O2 from female’s vascular system
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Reproductive modes:
anurans
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Parental care - Eggs imbedded
in skin of female
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Parental care - Darwin’s frog
~Rhinoderma darwinii
Terrestrial eggs hatch and are
carried by males in their vocal
sacs until they complete
metamorphosis
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Birth of a gastric-brooding frog (Rheobatrachus
silus)
Parental care ~ Coqui
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When males are experimentally
removed, only 23% of clutches
hatch (vs 77% in controls)
Die from desiccation (43%),
cannibalism from other males
(32%), and predation by
invertebrates (4%)
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Parental care is highly derived in many dendrobatid species, including
use of phytotelmata (water containers in bromeliads or tree holes) and
feeding with unfertilized eggs.
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Reproductive
modes:
Direct
development
Turtle Frog
Myobatrachus gouldii
Australian – arid zone
Direct development deep in burrow
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Reproductive modes: anurans
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Internal fertilization occurs only in a few species
E.g. Ascaphus truei (tailed frog)
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Fast moving waters
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Hybridogenetic waterfrogs: European
waterfrog complex (kleptons)
Pelophylax esculenta
Common edible frog =
Pelophylax ridibundus
(Marsh frog) X
Pelophylax lessonae
(Pool frog)
• Combine in some
areas: females mate
with males of either
species but discard
male genome
• Female-only lineages
of esculenta
• Larvae more fit under
some conditions
• ridibundus and
lessonae typical
lineages
Alternative development strategies
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Figure 8.30 Paedomorphosis in
Ambystoma
Heterochrony
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The difference between timing of
development between an ancestral form and
a derived one
Paedomorphisis or neoteny is a prime
example
Metamorphosis in salamanders is simply shut
down at a very early age while other
developmental process, e.g. gonad
maturation, continue
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Cause of heterochrony
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Delayed secretion of the thyroid hormone thyroxine
will result in delayed metamorphosis
Results in larval somatic traits never lost although
sexual maturation and large size still attained
This developmental switch can cause divergence
between species, e.g., Ambystoma mexicanum and
A. tigrinum
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Wild type (above) and lab strains (below)
Axolotl or Mexican Salamander
(Ambystoma mexicanum)
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Variation in Neoteny within Species
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Notably, sometimes
seen within the
same species and
even among local
populations – i.e.,
not obligate
Notophthalmus and
Ambystoma are
good examples.
What are those
evolutionary
reasons?
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Facultative neoteny in Notophthalmus
viridescens
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Balancing the risk of metamorphosis versus
that of remaining in the aquatic habitat
Larvae may be 'forced' to metamorphose if
there is a lack of food in the aquatic habitat or
if that habitat is in danger of desiccation
But eft and adult stages
are not seen in some
Long Island and Cape
Cod populations. Why?
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Evolutionary Selection Pressures
Larval habitat permanent Larval habitat temporary
Eft
habitat
poor
Eft
habitat
good
Neoteny favored
No newts
-Cape Cod, Long Island
(is bad newts!)
Neoteny
occasional
Metamorphosis
favored (typical
mode)
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When neoteny becomes viable
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Can prevail in populations inhabiting
permanent aquatic habitats where fishes are
rare or absent with uplands inhospitable for
efts
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Paedomorphosis in plethodontid salamanders is
associated with cave-dwelling
End: Amphibian Reproduction
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