International Association for Ecology

Life Cycle Polyphenism as a Factor Affecting Ecological Divergence within Notophthalmus

viridescens
Author(s): Mizuki K. Takahashi and Matthew J. Parris
Source: Oecologia, Vol. 158, No. 1 (Nov., 2008), pp. 23-34
Published by: Springer in cooperation with International Association for Ecology
Stable URL: http://www.jstor.org/stable/40309701
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Oecologia (2008) 158:23-34
DOI 10.1007/s00442-008- 1125-8

PHYSIOLOGICAL ECOLOGY - ORIGINAL PAPER

Life cycle polyphenism as a factor affecting ecological divergence

within Notophthalmus viridescens

M izuki K. Takahashi • Matthew J. Parris

Received: 18 September 2006 / Accepted: 26 July 2008 / Published online: 16 August 2008
© Springer-Verlag 2008

Abstract Polyphenism, which allows a single

eftsgenotype
under drying conditions but metamorphosed direct
aquatic
to express multiple discrete phenotypes in response toadults
envi- or became paedomorphic in constant wa
Also, N.envi-
ronmental cues, is an adaptive trait in heterogeneous v. viridescens metamorphosed to efts faster a
ronments. Pond hydroperiod is an importanta ecological
smaller body size than the other two subspecies. T
data
parameter affecting amphibian life history, and suggest
variation in that subspecies of N. viridescens are ad
local pond hydrology has been hypothesized to
to play a rolepond hydroperiods, supporting the potenti
different
in species divergence via changes in polyphenism. The to facilitate divergence. Canalizing sele
polyphenism
eastern newt (Notophthalmus viridescens) expresses lifealternative phenotypes within a single spec
for certain
cycle polyphenism. Larvae develop along three
whichpossible
other populations remain plastic may play an im
tant via
pathways: metamorphosis to aquatic lunged adult rolea in the initiation of ecological divergence.
ter-
restrial juvenile (eft) stage, metamorphosis directly to an
aquatic lunged adult, or maturation directly Keywords Adaptation • Ecological divergence •
to an aquatic
Life cycle polyphenism • Pond hydroperiods •
gilled adult without metamorphosis (i.e., paedomorphosis).
Salamanders pat-
Subspecies of N. viridescens vary in their polyphenic
terns, suggesting possible adaptation to different environ-
ments. However, no studies have experimentally tested
Introduction to
how genetic and environmental components contribute
the observed differences among subspecies and whether
such differences may facilitate divergence. We selection
Natural tested can drive phenotypic divergence in eco-
whether adaptation to local pond hydrology via polyphenic
logically important traits. Consequently, reproductive isola-
changes existed among subspecies by rearing larvae
tion could of as a by-product of adaptation to distinct
evolve
environments,
three subspecies (N. v. dorsalis, N. v. louisianensis, and N.leading to ecological divergence (Rundle
etal. 2000;
v. viridescens) along three hydroperiod regimes Schluter 2000, 2001; Coyne and Orr 2004).
(short,
Selection
long, and constant) in outdoor artificial ponds. may favor phenotypic plasticity under variable
We found
environmental to
that larval N. v. viridescens obligately metamorphosed conditions (Scheiner 1993; Van Buskirk and
Relyea
efts under all hydroperiods, whereas N. v. dorsalis 1998;
and N. Pigliucci
v. 2001), whereas consistent divergent
selection couldto
louisianensis exhibited plasticity: larvae metamorphosed lead to a limited range or loss of plasticity,
potentially facilitating evolutionary divergence (Losos
et al. 2000; Price et al. 2003; David et al. 2004). Although
divergence might be impeded by continuous plastic
Communicated by Kouki Hikosaka. responses, polyphenism, a type of plasticity in which a
genotype produces discontinuous alternative phenotypes in
M. K. Takahashi (IS) • M. J. Parris
response to different environmental conditions, has
Department of Biology, University of Memphis,
Memphis, TN 38152, USA received much recent attention as a potential ecological
e-mail: mtakahsh@memphis.edu mechanism affecting species diversification (Roff 1996;

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 24 Oecologia (2008) 1 58:23-34

Smith and Skulason 1996;

hydroperiods, Pf
a
West-Eberhard 2003;
rapidlyDenoél
and et
met
Polyphenism experiencing
may facilitate long
ins
distinct 2000). within
phenotypes Persistent
a sp
If consistent divergent
imposed selection
by short
phenotypes in in a
some fixed respon
populations
natives in costs
others, involved
genetic in
diver
occur (West-Eberhard
1998). In1986; Ma
contras
nig and
Murphy
pond2002; West-Eb
hydroperiod
adaptive larval
genetic developme
divergence is a
ical and behavioral changes,
polyphenic amby a
morphs may tigrinum,
facilitate and A.
divergenc
(Bush 1994). under
For drying
example, aq
body
spine aquatic
sticklebacks habitats.
{Gasterosteus
adaptations advantageous
for alternative in
for
assortative can
mating have a
betweengreate
diff
laboratory rapid growth,
experiments, ear
sugges
(Nagel and metamorphic
Schluter 1998). adu
Polyphenism etal.
is 1990; in
common Whit
am
excellent Ryan
models forand Plague
understand
by differentialmorphs can
polyphenic vary
expr
and Collins 1997; Larson
Eastern et al. N
newts, 1
2003). Life cycle
cycle polyphenism
polyphenism (e
phosis) within in
widespread N. salaman
virides
is
tion for certain
and alternativ
the expressi
hypothesized (Table
as a 1). Develop
mechanism f
and Armentrout 1976;
ways: (1) Shaffe
metamo
West-Eberhard 2003).
through Previous
a terrest
divergence directly
facilitated to
by a lun
polyph
on proportionalgilled aquatic
changes in adu
differ
among populations within
phosis). Fitnessth
t
Armentrout 1976;
are Semlitsch
evident in an
N
et al. 1990; selection
Denoél et al.should f
2001b).
tionary ofescape
life desiccati
cycle roles
polyph
ied, especially in populations
juveniles, however
Ambystoma because
talpoideumaquatic en
(Sem
Semlitsch 1987a, b;growth
nile Semlitsch a
(Hea
etal. 1990). nent water
However, or
althoughl
dence that life viridescens
cycle can
plasticityre
i
these studies did not provide
post-hatching bye
driven stage
divergence. To(Harris
date, 198
ther
logical require
divergence 3-7
via years
polyph
insufficient. maturation
Specifically, into p
evide
alternative the eft
phenotypes stage pre
within a
precursor to permanent
ecological aquat
divergen
Pond The influences
hydroperiod typical life
th
of adult newt) involves
pond-breeding amphib pa
development cycle
of may
larval reflec
pond-br
fore, it plays ronments.
an In role
important con
(Semlitsch et (peninsula
al. 1996; newt)
Wellborn
1999). stage
Freshwater and hydrop
lentic matur
a gradient adults,
from may be
quick-drying se
aquatic tions.
environments Plastic life
(Wellbor

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Oecologia (2008) 158:23-34 25

newt) and N. v. louisianensis (central newt) suggest

tions to varying or unpredictable pond hydrop
Although a great deal of studies has delineated varia

* I alii I life cycle polyphenism within N. viridescens (Table

studies have experimentally tested how genetic and
ronmental components contribute to the observed d
SSaI =
1ai
=a"Üj!
^a ^s^
s ÍÍ 4d
4I I| -g
S| I ^^ ences in the expression of alternative phenotypes a
subspecies.
In the study reported here, we tested to what exten
cycle variation in the broadly distributed and pheno
cally divergent salamander species - N. viridescens -
to local adaptation (genetic divergence). We aske

•I I Í question "are the subspecies of N. viridescens adapt

different pond hydrologies across their ranges"? If
predicted that either (1) some subspecies have ca
life cycles while others remain plastic, or (2) subsp
have plastic but different patterns of expression of al

I lililí -c off tive life cycles. If differences in polyphenic expre

i i S f í i ii-j i 1 1 among the subspecies are largely environmentally in

all should respond to a similar set of environmental
the same manner. If this is the case, we will have

i rfiili list in
dence for genetically based differences, and thus loca
tation is unlikely. We conducted an artificia

i i .umüfü su experiment in which we reared larvae of three subs

N. v. dorsalis, N. v. louisianensis, and N. v. viridesc

H Hfüfffii H! along a hydroperiod gradient and tested for subsp

differences in the expression of alternative phenotype

1 1 |t I* f -i M ■ i -i vival, growth, and development of larval newts.

If I1!111!11! ill
i Hi Materials and methods

C W) O ON ^
•Í !w 2 8 8 * -8 Source populations and breeding design
s « e ^ 7 7 7 y •£ £
o) .2 -S1* « The distribution ranges of eastern newt subspecies can be
•a -a c * defined by natural regions (Fig. 1; Duellman 1999). A natu-
ral region is a continuous geographic unit which experi-
ences similar climatic conditions and possesses
8- -8 ÜI 1 1 >16-
1 I s-* ! I ^|g characteristic types of vegetation. Therefore, a natural

1 | I || ¡ | |%|
"o *OGW)»-i O *S ON C
region can be viewed as a geographical unit suitable for
certain amphibian species (Duellman 1999). For example,
N. v. viridescens is predominantly distributed in the Appa-
1 !£i! 11 1 i|S lachian Highlands and the eastern Laurentian Upland, with
sí |l-2 Sil -tí I a
I sí I II II! If i! 5*J
a peripheral distribution extending into the Northern
Coastal and Interior Plains. Notophthalmus. v. louisianensis
I * e ? 8 £¿? ^ S ÍÍ Z|£ is distributed in the Interior Plains and the southern part of

^Q
^Q2ffl<
r^
g 1-3 Z
^§5
«
s& S-8 £ in
ZTl|g
43
rg
the Atlantic Coastal Plains, whereas N. v. dorsalis is found
the Atlantic Coastal Plain in South and North Carolinas
cm

í r^ « ¡F 43 cm (Fig. 1). Accordingly, we sampled three subspecies of east-

ern newt (N. v. viridescens, N. v. dorsalis, and N. v. luisian-
5 5 I 118 81 ensis) from core areas of each subspecies distribution: the

ÍÍÜ 1 I ill Appalachian Highlands for N. v. viridescens, the Interior

Plains for N. v. louisianensis, and the Atlantic Coastal

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 26 Oecologia (2008) 1 58:23-34

of adult N. v. loui
March we collecte
pond (35°58'N, 9
which is part of t
as the original per
permanent pond p
malswere returne
Meeman Biologica
Tennessee (35°22
We established
types x three su
population was m
(polyethylene c
approx. 2300 L) f
water and contain
added two snails
collected from ne
different times) t
position by natur
H. versicolor, and
for salamanders.
Fig. 1 Range of Notophthalmus
collected virides
animals
natural regions (Duellman 1999), and sa
natural regions
ing
are
populations.
delineated by heav
O
follows: / Interior June //
Plains, 2003. Ovip
Appalachian
al Plain, and breeding
/VLauretian populati
Upland. /, 2,
salis, N. v. viridescens, and N. v. louisi
ers (3 L) submer
hatching.
Plains for N. v. dorsalis (Fig. 1).
mals from Experimental design
peripheral population
boundaries to exclude individu
adapted to We tested for differences among subspecies, natal pond
underrepresented mar
avoid samplingtypes (temporary or permanent) nested within subspecies,
intermediate gen
Previous hydroperiods,found
studies and their interactions on thesignific
expression of
phenic alternative phenotypes,
expression among growth, and development of larval
populat
were newts. The three main factors
geographically and their interactions were loca
closely
different hydroperiods design.
examined in a randomized factorial Hydroperiod
(Semlitsc
litsch etal. 1990). Therefore,
regimes consisted of: (1) a short hydroperiod treatment (8- it i
history week drying)
variation notsimulating temporary
only ponds havingamong
the short-
subspecies. est hydroperiod
We sampled under which N. viridescens larvae can
adult n
from two metamorphose to efts (Bishop
different ponds1941), (2) a long hydrope-
with
(ephemeral andriodpermanent)
treatment (16-week drying) simulating hydroperiods
withi
Ephemeral ponds
correspondingdry annually,
to the longest larval period reported for the
hold water species (Harris
year around. et al. 1988), and (3) a constant
Thus, water treat- in
adult N. v. ment simulating permanent
dorsalis (ten ponds.females
We had two replicates a
temporary (35°02'N, 79°40'W)
per natal pond type within subspecies; thus, each subspe-
(35°O3'N, cies main factor was
79°38'W) in replicated four times. We randomly
Richmond
(21 March), assigned treatment
adult N. combinations
v. to 36 virides
artificial ponds
(38°18'N, 82°20'W) and1300L)
(diameter 1.83 m, volume approximately perm
in an
82°19'W) in Wayne
array at MBFS. Each pondCounty,
was equipped with an internal W
and adult N. v. louisianensis
movable standpipe to standardize and adjust water depth. f
(36°28'N, We filled each pondin
91°19'W) with approximately
Randolph 950 L (depth
permanent pond (36°31'N,
36 cm) of tap water 91°2
and added 1 kg homogenized air-dried
Missouri (15 leaf litter to each pond Because
March). on 25-26 April. A mixture of of

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Oecologia (2008) 1 58:23-34 27

zooplankton long
collectedhydroperiod
from local
was added in equal volumes
domorphs of (1.5
N. vL
before and at the beginning
All of dr
completely th
food sources for larval
remaining salaman
animals
Two snails of initially
(Lymnidae) were stocke
releas
late natural aquatic
pond adult,
dynamics onbeca
21
with screen lidsat
tothe end
prevent of the
coloni
tors and for
ovipositioncollected
by efts.
anurans.
natural individuals
photoperiod and and cla
temperatu
Initial larval terrestrial
density was juvenile
5.66 larv
L (ten larvae per tank), We
domorph. which
cons
observed in natural pondsthat
individual (Harris
rem
Because newts a dorsal asynchron
oviposit tail fin.
populations immature
over several individu
months,
nously. skin and
Consequently, welacking
introd
ments in an early
an and late
aquatic temp
metamo
1987). On 24 May,
mal early larvae
remaining in
tanks, and on 09 June,
such as late
gills larvae
and a
remaining 18 ually
tanks. mature
We did aqua
not
contributed to the egg
teristics stocks
yet an f
ov
derived. However, a subsequent
determined malese
spring 2006 an enlarged
following the cloaca
same
females (n = 10) that
surfacewere
of kept
the thi
allowed to matelacked
with males
these (n =
chara1
viable eggs. converged
Also, females on the
potentia
by males in sected
their animals
natal ponds and
bef
females ing
typically secondary
mate with se
sever
ing seasons (upbased
to 6 on the prese
months; G
Therefore, it issperm
likely in males.
that the la
ment provided sufficient genetic d
population-levelData analyses
responses.
Pond water levels were reduced e
tally lowering We
the used multivar
internal stand
the short test fortreatment
hydroperiod the effect
long subspecies
hydroperiod differe
treatment, such
zero after 8 N.
and 16v. louisianensi
weeks, respec
the constant (permanent
water ponds or
was eph
kep
rainfall stant
compensating water),
for and
evaporat
the and
experiment. Wepond typeall
checked x
metamorphosinglength,
efts proportion
until the fi
Day 47); morphosis
thereafter, all to
pondseft.
we
week until the analyses
end of theofexperim
varian
typically were significant
collected oncontr
the f
ponds where the
the four dependen
recurved structu
escaping. We a
did significant
not check int
aquat
adults for hydroperiod
larval period on
and/or o
bo
sis data because VAs
it to
was comparison
an intracta
these traits on tors (e.g.,
animals thateach hy
remain
out the the
experimentsubspecies
without x h
dist
mesocosms. Weresponses.
ended the For exa
experi
found the last sons
eft (10of larval
November;pe
tal period was hydroperiod
also chosen (shor
becau
that animals subspecies
remaining in x hydr
constant

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 28 Oecologia (2008) 158:23-34

Table 2 Summaryaddition,
of pond type,
MANO nor the interaction between
VA pond type
for ov
addition, subspecies differences,
and hydroperiod had a significant multivariate effect on lar- pond
and hydroperiod on survival, proporti
val responses (Table 2). Consequently, we tested the effects
ing to eft, larval period of individuals m
mass at of subspecies, hydroperiod,
metamorphosis to and theireft
interaction onfor
univar- N. v
iate larval responses (Table 3).
Source of variation df Wilks' F P
lambda
Larval survival was not significantly affected by any
main effects or interactions (Table 3). There were signifi-
Date of larval addition 4,19 0.613 1.42 0.3038 cant effects of subspecies and hydroperiod on the propor-
Subspecies 8,38 0.178 3.09 0.0224 tion of individuals metamorphosing to eft. A significantly
Pond type (subspecies) 12,51 0.175 1.88 0.0914 greater proportion of N. v. viridescens larvae metamor-
Hydroperiod 8,38 0.035 9.85 <0.0001 phosed to efts than either N. v. dorsalis or N. v. louisianen-
Subspecies x hydroperiod 16,28 0.094 2.06 0.0459 sis; N. v. dorsalis and N. v. louisianensis did not
Pond type x hydroperiod 24,33 0.203 0.79 0.7248 significantly differ in eft production (Table 3; Fig. 2a). Lar-
vae metamorphosed to efts more frequently under the long
MANOVA, Multivariate analysis of variance
hydroperiod than in short hydroperiod or constant water
conditions.
Because no subspecies produced aquatic metamorphic
The larval period of individuals metamorphosing to efts
adults or paedomorphs under short hydroperiods, and N. v.significantly among subspecies and across hydrope-
varied
riods; N. v. louisianensis and N. v. dorsalis had similar lar-
viridescens larvae did not yield any aquatic metamorphic
adults or paedomorphs across all hydroperiod treatments,
val periods, which were significantly longer than that of N.
we conducted an additional MANOVA, excluding the v.short
viridescens (Table 3; Fig. 2b). Larvae metamorphosed to
hydroperiod treatment and N. v. viridescens, to test
eftsthe
significantly faster under short than long hydroperiod
effects of date of larval addition, subspecies differences,
or constant water conditions; larval periods under long
pond type nested within subspecies, and hydroperiod on
hydroperiod and constant water conditions were similar
proportions of aquatic adults and paedomorphs. We did
(Fig.not
2b).
include larval period and body mass for metamorphosis The body mass of individuals metamorphosing to efts
data in these analyses because it was an intractable also
proce-
varied significantly among subspecies and hydroperi-
dure to measure these traits on animals that remained in the ods and followed a similar pattern to that of larval period
water throughout the experiment. We performed subse- (Table 3; Fig. 2c). The body masses of N. v. louisianensis
quent ANO V As to determine the effects of significant con- and N. v. dorsalis at metamorphosis to efts were similar and
tributors detected in MANOVA on these two responses. also significantly larger than that of N. v. viridescens. Over-
We used Tukey's studentized range tests for all pairwise all, all three subspecies attained greater mean body masses
comparisons in post hoc analyses. under long hydroperiod and constant water conditions than
under the short hydroperiod, and body mass between long
hydroperiod and constant water conditions did not signifi-
Results cantly differ (Fig. 2c). A significant interaction between
subspecies and hydroperiod suggested that subspecies
Eft responses responded differently to the hydroperiod treatments. Eft
body mass for N. v. viridescens was similar across all
Subspecies, hydroperiod, and the interaction between sub- hydroperiod treatments. Under the short hydroperiod and
species and hydroperiod were significant contributors to constant water conditions, the three subspecies had similar
overall larval responses (Table 2). Neither date of larval body masses (short F25 = 0.83, P = 0.49; constant

Table 3 Summary of ANO V As for effects of date of larval addition, subspecies, pond type nested within subspecies, and hydroperiod on survival,
proportion of individuals metamorphosing to eft, larval period of individuals metamorphosing to eft, and body mass at metamorphosis to eft for
N. viridescens subspecies

Source of variation Survival Eft proportion Larval period Eft body mass

df F P df F P df F P df F P

Subspecies 2 1.04 0.366 2 12.20 <0.001 2 7.74 0.003 2 8.49 0.002

Hydroperiod 2 2.36 0.114 2 13.18 <0.001 2 19.23 <0.001 2 7.79 0.003
Subspecies x hydroperiod 4 0.10 0.981 4 2.46 0.071 4 2.12 0.113 4 3.02 0.040
Error 27 26 22 22

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 Oecologia (2008) 1 58:23-34 29

Fig. 3 Proportions of alternative phenotypes (eft, direct metamorpho-

sis to aquatic adult, or direct maturation to paedomorph) and individu-
als that remained as larvae of the eastern newt subspecies (Subspp: N.
v. louisianensis, N. v. dorsalis, N. v. viridescens) under three hydrope-
riod treatments (Hydro): short, 2 month drying; long, 4 month drying,
constant, constant water, 5 months

Discussion

Demonstrating how divergent selection imposed by

environmental factors leads to genetic divergence of pheno-
typic traits is the first step in testing ecologically driven
speciation (Schluter 2001). The results of our experiment
demonstrate that subspecies of the eastern newt may be
Fig. 2 The effects experiencing
of ecological divergence. In our
subspecies experiment,
[Subspp
dorsalis (D), N. v. viridescens
subspecies, hydroperiod, and their(V)\ and
interaction had signifi- th
(Hydro-, short drying,
cant effectslong drying,
on overall larval consta
responses, suggesting that
b larval period, c body mass of individu
Error bars Standard error different subspecies of N. viridescens adapt to different hyd-
roperiods by altering polyphenic expression, growth, and
development. Larvae of N. v. viridescens consistently meta-
F2 8 = 4.18, P = 0.06), while under the long hydroperiod, N.morphosed to efts under all hydroperiods, suggesting a lack
v. dorsalis and N. v. louisianensis had larger body masses of polyphenic plasticity for this subspecies, at least in the
than N. v. viridescens (F29= 13.16, /><0.01); the bodypopulations we sampled. In contrast, N. v. louisianensis and
sizes of N. v. dorsalis and N. v. louisianensis were not sig-N. v. dorsalis exhibited developmental plasticity, and facul-
nificantly different. tatively adjusted their life cycles depending on prevailing
hydroperiods: N. v. louisianensis and N. v. dorsalis pos-
Metamorphosis to aquatic metamorphic adult sessed greater degrees of plasticity than N. v. viridescens
and paedomorphosis along a hydroperiod gradient for continuously (larval
period and body mass at metamorphosis to eft) as well as
Hydroperiod was the only significant multivariate effect ondiscretely plastic (polyphenic expression) traits.
larval responses (Wilks' Lambda = 0.307, F2 6 = 6.76, Age at maturation is the principal target of natural
P = 0.0291). The univariate hydroperiod effect was signifi-selection in the evolution of aquatic gilled adults of ambys-
cant on both the proportion of paedomorphs (F, 14 = 8.89, tomatid salamanders (Ryan and Semlitsch 1998). In Not-
P < 0.01) and aquatic metamorphic adults (F,,4 = 5.71,ophthalmus, efts typically spend 3-7 years in terrestrial
P = 0.03). While N. v. viridescens did not yield any aquatic environments before moving to breeding ponds and attain-
metamorphic adults or paedomorphs, significantly more ing sexual maturity (Table 1). Our histological examina-
paedomorphs and aquatic metamorphic adults were pro- tions of follicle and sperm development indicated that N. v.
duced under constant water conditions than long hydrope-louisianensis and N. v. dorsalis that directly became meta-
riod ones in N. v. louisianensis and N. v. dorsalis (Fig. 3). morphic or gilled adults were sexually mature within

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 30 Oecologia (2008) 1 58:23-34

5 months after
Despite hatching.
the strong philopatric behavior of adultThus,
newts (Gill
habitats are available, life
1978; Phillips 1986), N. viridescens cycle
has a widespread dis-
greater reproductive advantages
tribution (Fig. 1), which suggests that dispersal from natal
N. v. dorsalis. ponds occurs in eastern newts during terrestrial stages. A
Our results also demonstrate genetically based differ- long eft stage, coupled with aposematic coloration and
ences among subspecies in continuously plastic traits,highly toxic skin (Brodie 1968), likely enables frequent and
namely larval period and body mass at metamorphosis to long-distance dispersals. For example, Gill (1978) reported
eft, which correlate with each other (r = 0.666, P < 0.0001 that all of five newly constructed ponds became colonized
in our study). Overall, N. v. viridescens metamorphosed toby a large number of adult newts within 10 years of con-
efts more rapidly, but at a smaller body size, than the other struction. These ponds were located at some distance (sev-
two subspecies; N. v. louisianensis and N. v. dorsalis eral kilometers) from the nearest available source ponds,
remained in the aquatic environments longer but attained suggesting that long and frequent overland dispersal made
larger body sizes. Therefore, under rapid-drying conditions, colonization events possible (Gill 1978). Data from two
N. v. viridescens performed better by producing more eftsgenetic studies also support high terrestrial dispersal ability.
quickly; however, under long hydroperiods, the other twoMerritt et al. (1984) found unexpectedly high levels of het-
subspecies were able to take advantage of the high-growtherozygosity within coastal paedomorphic populations of N.
aquatic environment more efficiently (Healy 1973, 1974). v. viridescens as well as high levels of genetic similarity
Notophthalmus v. viridescens may therefore have an advan-between coastal paedomorphic and inland metamorphic
tage in regions where permanent and semi-permanent ponds populations in the northern USA. Reilly (1990) found
are scarce. In these regions, rapid metamorphosis to terres-lower genetic variation within N. viridescens than expected
trial efts enables newts to utilize a wider range of aquatic for a wide-ranging species. Although currently available
habitats, including quick-drying seasonal pools. In contrast,empirical and observational data on the terrestrial dispersal
in regions with abundant permanent and semi-permanent of newts are insufficient, these results suggest that terres-
water, quick metamorphosis is not essential, and thus indi-trial dispersal among populations of eastern newt occurs
viduals that reach sexual maturation faster by remaining infrequently, which likely explains the similar responses of
the water longer likely have selective advantages. larval newts derived from different pond types within sub-
It is important to note that our experimental design didspecies.
not allow us to preclude the possibility of nongenetic Pond hydroperiod is an important environmental factor
maternal effects on polyphenic expression. However, such for pond-breeding amphibians, and local populations are
effects are likely to be negligible. For example, althoughadapted to prevailing hydroperiod regimes (Semlitsch et al.
variation in egg size can lead to variation in early larval 1996; Wellborn et al. 1996; Skelly et al. 1999). In faculta-
growth rate, variation in the mean growth rate of larval A. tively paedomorphic salamanders, the results of earlier
talpoideum did not affect the expression of alternative studies suggest the importance of pond hydroperiod as both
developmental phenotypes (Semlitsch 1987b). In our a proximate and ultimate causes of changes in life history
experiment, larval growth rate did not differ among subspe-polyphenism (Rose and Armentrout 1976; Semlitsch and
cies (F2 17 = 0.60, P = 0.56). Harris (1987) also found simi-Gibbons 1985; Semlitsch and Wilbur 1989; Semlitsch et al.
lar patterns of polyphenic expression in N. v. dorsalis1990). In our study, hydroperiod had strong effects on both
across two artificial pond experiments conducted in differ-the life cycle and life history responses (i.e., larval period
ent years with different breeding populations, suggesting aand body mass) of larvae, and the significant interaction
low potential of maternal effects on polyphenic expression. between subspecies and hydroperiod suggests that subspe-
Significant differences in polyphenic expression amongcies are likely adapted to different hydroperiods. Direc-
closely situated populations of A. talpoideum were reportedtional and persistent selection potentially could cause a
in earlier studies (Semlitsch and Gibbons 1985; Semlitsch developmentally plastic pathway to become fixed (Sem-
etal. 1990). In our study, however, larval newts derived litsch and Wilbur 1989; DeWitt et al. 1998; Pigliucci 2001;
from different pond types (ephemeral or permanent) exhib- Schlichting 2004). Both the obligate metamorphosis to eft
ited similar responses within subspecies. One of the major and the short larval periods of N. v. viridescens suggest can-
differences in life cycle between N. viridescens and A. tal- alizing selection for short developmental periods and meta-
poideum is the eft stage of N. viridescens. Whereas meta- morphosis to a terrestrial life form. In contrast, the greater
morphosed A. talpoideum become sexually mature within adevelopmental plasticity in N. v. louisianensis and N. v.
few months of metamorphosis and breed during their firstdorsalis suggests unpredictability and heterogeneity in their
year (Petranka 1998), metamorphosed efts of N. viridescensaquatic habitats (Wilbur and Collins 1973).
typically spend 3-7 years in terrestrial habitats before Wetland distributions (Babbitt and Groat 1998) and soil
entering breeding ponds as sexually mature individuals. drainage classes (Aiguo and Changai 2001) roughly corre-

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 Oecologia (2008) 158:23-34 31

spond to the subspecies distribu

designed our experiment to elucidate the typical life history
reflected by of each subspecies.
physiological natur
Wetlands are scarce, and
Previous models of amphibian well-d
metamorphosis suggest
throughout thethat both
most terrestrial and aquatic
of environments
the influence
south
the
and the eastern
life history
margin
of amphibians (Wilbur and of
Collins 1973;the
Wer- I
Groat 1998; Aiguo and
ner 1986), and the same Changai
likely holds true for N. viridescens.
viridescens is distributed infavors
The rarity of large, stable, fish-free aquatic habitats the
eastern margin of
fast metamorphosis the
to the terrestrialInterior
eft, thus enabling N. v. P
Plain north of viridescens
North to colonize quick-drying
Carolina, ponds. Favorable an
of the woodland environments
Laurentian Upland. in the Appalachian Highlands,
There
propensity forwhere terrestrial life histories
rapid are common in many pleth-
metamorph
its areas
lacking ice-free,
odontid salamanders perm
(Wilbur and Collins 1973), may also
consistent withfavorthe
the terrestrialview
eft stage of N. v. viridescens.
that In con- pon
tant factor in trast,
life cycle
in the Atlantic diverge
Coastal Plain and Interior Plains, ponds
lakes are relatively
with long hydroperiods common
or permanent water are relatively in
Atlantic Coastal
abundantPlain north
(Babbitt and Groat 1998), of
thus allowing N. v. dor- N
glaciated salis and N. v. louisianensis
terrain (the to exploit favorable aquatic
Finger L
Regions of environments;
New York, terrestrial environments
all lacking
of favorable
New
tian Upland of Canada)
woodland where
characteristics may select against the eft stage. In ex
tions created these regions, terrestrial plethodontid depress
numerous salamanders are
paedomorphic much
N. less common
v. and generally occur at lower densities
viridescens
the northern (Wilbur
Atlantic Coastal
and Collins 1973; Petranka 1998), providing fur- P
have not been observed
ther and
evidence of the effect of harsh ecological conditionsefts
on
glaciated the terrestrial
terrain. A lifedifference
stage of salamanders. This association in
tion to the between polyphenic expression
freezing point and habitat characteristics
betwe
dent: 0-5°C in the
has been suggested in ambystomatid salamanders in Atlan
northern North
- 15°C in the America (Rose and Armentrout 1976; Shaffer
Northern 1984; Sem-
Appalac
the glaciated litsch and Gibbons 1985; Ryan and(Duellma
terrain Semlitsch 1998). On
decreases below the
the other hand, freezing
ecological parameters of aquatic and terres-
freeze solid, and animals
trial environments do not explain the patternsin deep
of polyphenic
winter kills. Because N. viridescens is not freeze-tolerant expression in alpine newt, Triturus alpestris (Denoél et al.
and dies after 4 h of freezing at -2.5°C (Storey and Storey 2001a). Resource competition within populations likely
1992), the winter freeze of aquatic habitats is the functional explains maintenance of life cycle polyphenism in this spe-
equivalent to pond desiccation, which likely explains fre- cies (Denoél and Joly 2001; Denoél et al. 2004).
quent metamorphosis to the terrestrial eft in the glaciated Current data indicate that paedomorphic N. v. virides-
terrain despite its abundant wetlands. Winter freeze avoid- cens are found only in a northern part of the Atlantic
ance behavior was observed by Gill (1978), who found that Coastal Plain (Noble 1926; Bishop 1941; Healy 1970). The
newts repeatedly migrated from permanent ponds to terres- Coastal Plain environment is very distinct from the pre-
trial winter hibernacula in Virginia. Notophthalmus v. dor- dominant habitat of N. v. viridescens (i.e., the Appalachian
salis and N. v. louisianensis are distributed throughout the Highlands) in that the former contains harsh terrestrial
Atlantic Coastal Plain and the Interior Plains along the Mis- environments with a sandy floor and abundant aquatic habi-
sissippi River, where common and frequent wetlands and tats with long hydroperiods or permanent water. This com-
poorly drained soils are found (Babbitt and Groat 1998; bination may select for an aquatic life history in N.
Aiguo and Changai 2001). Our data suggest that these two viridescens. We suggest that the aquatic life history of the
subspecies are adapted to spatially and temporally hetero- coastal populations of N. v. viridescens is evidence of in
geneous hydroperiods and facultatively adjust life cycles situ ecological divergence via polyphenic changes within
depending on aquatic environments. While our experimen- subspecies. Alternatively, introgression from N. v. dorsalis
tal outcomes corroborate the patterns delineated by the may have made it possible for the coastal populations of N.
known life history of this species, applying our findings to v. viridescens to obtain a more aquatic life history. It has
regions that lack solid natural history data must be done been suggested that polyphenic expression has the major
with caution because little is known about how life history gene basis in A. mexicanum (Voss and Shaffer 1997; Voss
patterns change across subspecies boundaries. By sampling and Smith 2005; but see Voss and Shaffer 2000). If N. viri-
populations within the core areas of each subspecies, we descens shares a similar underlying genetic architecture for

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 32 Oecologia (2008) 1 58:23-34

their distinct expression,

polyphenic environments could facilitate ecological divergence
limit
the gene(s) among subspecies of N. viridescens.
underlying polyphenic
an aquatic developmental pathway
A recent phylogenetic study of N. viridescens based on
tion of N. v. viridescens and
allozyme data does not reflect current persi
subspecies taxonomy
Repeated changes
(Gabor and in
Nice 2004).polyphenic
Instead, these analyses support three s
multiple speciation events
geographical units: in
a Florida group, a Northern group,amby
and a
Mexico (Shaffer 1984),
non-cohesive Southern group.suggesting
Substituting the groupings of
polyphenism Gabor and Nicechange
could (2004) for currently accepted subspecies
repeate
The results of designations
our study
yields indicate
findings consistent with the patterns of
could affect genetic divergence
life cycle polyphenism that we found, namely: significant in
a manner that differences between
may N. v. viridescens and the other twodive
facilitate sub-
Whereas geographical
species. Specifically, ourvariation
work used N. v. viridescens from in
natives are commonly found
West Virginia, which is within the Northern group, and N. v. acr
directional dorsalis from North
selection Carolina and N. v.to
leads louisianensis
the from fix
tives in some populations while
Arkansas, both of which are in the Southern group of Gabor ot
within a singleandspecies is
Nice (2004). Thus, the patterns relativel
of divergent selection on
West-Eberhard 1986,
life history traits driven by 2003). Our
differences in hydrology
some of the observed in
first our study likely played a evolution
critical role in shaping the
fixation of an intraspecific
alternativephylogeny of N. viridescens. pheno
within a single species. Genetic
Overall, our results demonstrate that divergent selection po
tant precursors
imposed
of by localthe
hydrology is ainitiation
critical process driving
(Bush 1994), and divergent
intraspecific selectio
divergence within N. viridescens. Divergence
ductive isolation
may bedespite
facilitated by the differentialthe prese
expression of life cycle
flow (Schluter polyphenism
1996; in which Bush and
canalizing selection fixed a develop- Sm
1998;Schluter mental
1998). If
pathway in one subspecies assortat
(N. v. viridescens), while
genetic others possess plasticity.
differences in Although
polyphenismthe hypothesis of
descens may diverge from
polyphenism-driven divergence N. in
has been investigated v. d
ensis. Assortative mating
several amphibian systems, supporting evidence to date hasin
facilitated by size differences
been equivocal. amon
Our results indicate that divergent selection
may be a by-product of may
driven by different hydrologies differenti
- when coupled with
viridescens are size-assortative mating within subspecies - play
significantly an impor-
larger
ern newt subspecies.
tant role in the initialGiven
stages of speciation. the sm
cens at metamorphosis, the lar
subspecies is Acknowledgments to
likely We thank S.be
Okada, T. Okada,
caused A. Mann, M. b
Mann, S. Trauth, N. Yamada, and B. Wheeler for assistance in the
long terrestrial eft stage. On the
field, and B. Beck, A. Braswell, C. Hams, S. Hartley, and L. Watson
maturing efts of
for specific N. v.
information of the field dorsalis
sites. We are also grateful to N. Jor- is o
that at metamorphosis to
dan, L. McClaren, Y. Sugahara, and R. Towne adults,
for assistance with our
shorter eft experiment;
stage in A. Banker, F. Brem, A, Combs, Z. Felix,
Coastal PlainD. Outlaw, R. en
Outlaw, J. Petranka, A. Pierce, B. Resetarits, M. Venesky, G. Voelker,
1988). Male newts choose larger f
Y. Wen, and two anonymous reviewers for suggestions on early drafts
1985; Park et al.
of the 2005), and
manuscript; Y. Takahashi for creating Fig. 1;larger
the Arkansas
competition (Gabor et
Game and Fish Commission, North al. 2000),
Carolina Wildlife Resource Com- su
for mission, and West
size-dependent Virginia Division of Natural Resources for collect-
assortative matin
ing permits. This research was supported partially by a Sigma Xi
evidence of intraspecific
Grant-in- Aid of Research. assortativ
phs of polyphenic salamanders (D
eman and Semlitsch 2005; Whiteman etal. 2006).
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 Oecologia (2008) 158:23-34 33

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