Environmentally Cued Hatching across Taxa: Embryos Respond
toRisk and Opportunity
Karen M. Warkentin1,*,†
*Department of Biology, Boston University, 5 Cummington Street, Boston, MA 02215, USA;†Smithsonian Tropical
Research Institute, PO Box 0843-03092, Panama ´, Repu ´blica de Panama ´
From the symposium ‘‘Environmentally Cued Hatching across Taxa: Embryos Choose a Birthday’’ presented at the
annual meeting of the Society for Integrative and Comparative Biology, January 3–7, 2011, at Salt Lake City, Utah.
Synopsis Most animals begin life in eggs, protected and constrained by a capsule, shell, or other barrier. As embryos
develop, their needs and abilities change, altering the costs and benefits of encapsulation, and the risks and opportunities
of the outside world. When the cost/benefit ratio is better outside the egg, animals should hatch. Adaptive timing of
hatching evolves in this context. However, many environmental variables affect the optimal timing of hatching so there is
often no consistent best time. Across a broad range of animals, from flatworms and snails to frogs and birds, embryos
hatch at different times or at different developmental stages in response to changing risks or opportunities. Embryos
respond to many types of cues, assessed via different sensory modalities. Some responses appear simple. Others are
surprisingly complex and sophisticated. Parents also manipulate the timing of hatching. The number and breadth of
examples of cued hatching suggest that, in the absence of specific information, we should not assume that hatching
timing is fixed. Our challenge now is to integrate information on the timing of hatching across taxa to better understand
the diversity of patterns and how they are structured in relation to different types of environmental and developmental
variation. As starting points for comparative studies, I: (1) suggest a framework based on heterokairy—individual, plastic
variation in the rate, timing, or sequence of developmental events and processes—to describe patterns and mechanisms of
variation in the timing of hatching; (2) briefly review the distribution of environmentally cued hatching across the three
major clades of Bilateria, highlighting the diverse environmental factors and mechanisms involved; and (3) discuss factors
that shape the diversity of plastic and fixed timing of hatching, drawing on evolutionary theory on phenotypic plasticity
which directs our attention to fitness trade-offs, environmental heterogeneity, and predictive cues. Combining mecha-
nistic and evolutionary perspectives is necessary because development changes organismal interactions with the environ-
ment. Integrative and comparative studies of the timing of hatching will improve our understanding of embryos as both
evolving and developing organisms.
Most animals, including all sexually reproducing
multicellular animals and many asexual metazoa,
begin life as eggs. They thus spend their earliest,
and potentially most vulnerable, stages developing
within some structure of maternal origin. Across
taxa, a great diversity of extraembryonic structures
has evolved, from relatively simple fertilization enve-
lopes to elaborate jelly layers, egg shells, egg cases,
and sacs of various types. These extraembryonic
which embryos develop and mediate their interac-
tions with the outside world.
As barriers, egg capsules both provide protection
and impose constraints. For instance, they slow the
loss of water, exclude many natural enemies, and
protect a pool of resources for use by the embryo.
However, they also impede oxygen uptake, prevent
access to external food sources, determine spatial lo-
cation, and limit size. The details of protection and
constraints vary with factors such as the structure of
egg capsules, maternal provisioning, and environ-
mental context, but trade-offs are inevitable. As em-
bryos develop, their needs and abilities change,
Integrative and Comparative Biology, volume 51, number 1, pp. 14–25
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at Leiden University on September 30, 2011
shifting the balance between the constraints and pro-
tection of the egg capsule and the risks and oppor-
tunities of the outside world. When the cost/benefit
ratio is more favorable outside the capsule than
inside, embryos should hatch.
Across the diversity of animal species, hatching
occurs at a wide range of developmental stages, from
blastulae to specialized larvae to juveniles that look like
small adults. Even among closely related species, the
developmental stage at hatching can differ substan-
tially. The evolved diversity of developmental stages
at hatching is widely appreciated and presumably re-
flects variation in the history of selection on encapsu-
lated and posthatching stages. Selection on embryos
and hatchlings also varies with local environmental
context, so that from time to time, place to place,
and egg mass to egg mass, the best time to hatch is
not always the same. The extent to which the timing
of hatching varies among individuals, as a plastic re-
sponse to such environmental variation, is not as
Hatching has often been treated as a developmental
event that occurs at some fixed stage. Variation in de-
velopmental rate that generates variation in the timing
of hatching has been viewed largely as passive, an in-
evitable direct effect of factors such as temperature.
There are, of course, many exceptions to this, some
of which are well-known, but they have been studied
largely in isolation from each other, with comparisons
restricted to particular environmental contexts or taxa
(e.g., Martin 1999). The number and breadth of exam-
now accumulated, however, motivate a re-evaluation
of the general assumptions of fixed timing of hatch-
ing and passive variation. A broader comparative ap-
proach to the timing of hatching is needed.
This symposium includes case studies of ECH in
particular well-studied species (Ishimatsu, Martin),
Spencer, Warkentin, Whittington), and recent work
opening new areas for investigation (Miner, Oyarzun
and Strathmann, Reed). To set these contributions in
a larger context and facilitate comparisons across
taxa, I offer: (1) an initial framework for description
of patterns and mechanisms of ECH; (2) a brief
survey of the phylogenetic diversity of ECH, high-
lighting the range of environmental factors and
mechanisms involved; and (3) and a discussion of
factors affecting the evolution of ECH.
Patterns andmechanismsof ECH
As the exit from the egg capsule, hatching is funda-
mentally an ecological transition between life history
stages. It is also an event within the process of de-
velopment that can occur at different points, both in
time and in relation to other developmental events.
The developmental stage and timing of hatching may
be buffered from environmental variation, intrinsi-
cally variable (bet-hedging), directly affected by en-
environmental factors. For an integrative and com-
parative analysis of the timing of hatching, we need a
conceptual framework that can incorporate this di-
versity. One starting point is the concept of hetero-
kairy. This term was coined to describe individual,
plastic variation in the rate, timing, or sequence of
developmental events and processes (Spicer and
Burggren 2003; Spicer and Rundle 2007), as a paral-
lel to the evolutionary concept of heterochrony
(Gould 1977; Alberch et al. 1979; Raff and Wray
1989; Reilly et al. 1997). Heterokairy offers a general
framework for comparing mechanisms and patterns
of the timing of hatching, drawing attention to the
fact that development is not a single, consistent pro-
cess (Warkentin 2007). The hierarchical, modular
nature of development means that multiple underly-
ing processes and traits contribute to any functional
capacity, such as hatching competence. For each of
those components, the rate of development may be
accelerated or decelerated, and the onset or offset of
processes may be shifted forward or back (Alberch
et al. 1979; Reilly et al. 1997). Moreover, changes in
different components may be decoupled, altering de-
velopmental sequences (Spicer and Burggren 2003).
Hatching plasticity exists when environmental fac-
tors induce, cue, or directly cause variation in either
the developmental stage at which hatching occurs,
the duration of the embryonic period, or both.
This plasticity may be adaptive or nonadaptive. It
includes direct effects of the environment on devel-
opment, which may be inevitable results of physics
and physiology and/or the results of adaptive pro-
cesses. It also includes embryonic and parental re-
sponses to token stimuli that serve as cues to
ECH. Fixed hatching occurs at a consistent stage in
development or, potentially, after a consistent em-
bryonic period, regardless of environmental condi-
tions. Presumably, this results from a canalization
process, in which the timing of hatching becomes
buffered from environmental effects.
We can delineate several possible patterns and
mechanisms of variation in the timing of hatching,
recognizing that more than one mechanism may
pertain in particular cases. If hatching occurs consis-
tently at a fixed point in development, altering its
timing requires altering the rate of development.
at Leiden University on September 30, 2011
This can, however, happen in different ways. Figure
1A illustrates multiple ways to delay hatching. Some
environmental factors, such as temperature, directly
affect embryonic development rate, and the same
factor may continue to affect posthatching develop-
ment [Fig. 1A(2)]. Different developmental processes
may, however, be affected to different extents, caus-
ing phenotypic variation in hatchlings (Kaplan
1992). Consistency in embryonic period and hatch-
ling phenotype requires the evolution of develop-
mental insensitivity to such effects, or canalization.
Embryonic development rate can also be tied
effect [Fig. 1A(3)], for instance it can be slowed
in responseto starving
(Voronezhskaya et al. 2008) or accelerated in re-
sponse to more advanced embryos in the nest
(Brua 2002; Spencer and Janzen 2011). Cued changes
in development rate will often be limited to partic-
ular developmental periods. The period of plasticity
in rate may include much of embryonic develop-
ment, starting as soon as sensitivity to the cue de-
velops. It may also be quite restricted; for instance,
some embryos develop at a consistent rate until
hatching competence and then wait for a cue to
hatch, slowing metabolism and development to pro-
long the period of readiness to hatch [Fig. 1A(4);
Martin et al. 2011; Whittington and Kearn 2011].
In some cases, hatching will not occur without the
cue and embryos die when energy reserves become
exhausted. At the extreme, periods of developmental
stasis, or dormancy, may occur (Andrewartha 1952;
Wourms 1972; Gyllstro ¨m and Hansson 2004). If en-
vironmental conditions directly limit development,
this is considered quiescence; if dormancy is endog-
enously maintained, even when conditions permit
development, it is diapause (Kostal 2006). In some
cases, hatching is decoupled from the termination of
egg dormancy by a substantial intervening period of
development [Fig. 1A(5)]. In others, hatching follows
closely upon the end of dormancy; thus the environ-
mental cues or conditions for hatching and the ter-
mination of dormancy must be congruent or
identical [Fig. 1A(6)].
The developmental stage at hatching can also vary
while development rate remains consistent (Fig. 1B).
Under certain conditions, embryos hatch spontane-
ously at a particular stage. Under other conditions,
an environmental cue may delay hatching, causing
embryos to hatch later in development, or stimulate
hatching at an earlier point, when embryos are less
developed (Warkentin 2011). Such plasticity gener-
ates coupled changes in the timing of hatching and
the phenotypes of hatchlings. Cued changes in stage
that haveno direct
Fig. 1 Patterns and mechanisms of variation in the timing of
hatching (modified from Warkentin 2007). (A) Multiple
mechanisms underlying delays in hatching with a consistent
phenotype of hatchlings, relative to (1) early hatching under other
conditions. Overall embryonic development may be slowed due
to (2) direct effects of the environment, which may continue after
hatching if animals remain in the same environment, or (3) as
a cued response of embryos, in which case the change in rate
is likely to be limited to particular stages. Direct effects and
cued responses may also accelerate development. (4)
Hatching-competent embryos may slow development while
waiting for a cue to hatch or (5, 6) a period of egg dormancy may
delay hatching. The end of dormancy may be decoupled from
hatching (5) or closely linked to hatching (6). (B) Variation in the
developmental stage of hatching, leading to coupled variation
in the timing of hatching and the phenotypes of hatchlings.
(C) Flexible timing of hatching depends on multiple traits that
enable survival and development in the egg capsule (e.g. 1, 2) and
outside environment (e.g. 4, 5), as well as the hatching process
(e.g. 3, 4). With modularity, the relative timing of different
developmental processes and trait functions may vary indepen-
dently. The onset of hatching competence (Hearliest) depends on
traits required for both hatching and life outside the egg.
Similarly, the end of the plastic hatching period (Hlatest)
may be determined by traits affecting hatching or survival
within the egg. Opposing selection pressures that favor
plasticity in hatching (bold arrows) will be focused on
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at hatching may occur by different mechanisms. For
instance, early hatching could occur if an acute stim-
ulus, such as attack by a predator, triggers hatching
at some point before the embryo would hatch spon-
taneously (Warkentin 1995). Delays may be caused
by a temporary inhibiting factor that prevents hatch-
ing from occurring when it otherwise would; hatch-
ing then occurs when the inhibition is lifted. For
instance, the emergence of eggs into air inhibits
hatching in some species of fish (Yamagami 1988).
Either developmentally early or delayed hatching
could also occur if an environmental factor, which
might be continuously present, shifts a developmen-
tal threshold or set-point for hatching. For instance,
green frogs hatch earlier in response to chemicals
from egg-eating leeches and later in response to
chemicals from odonate predators of larvae (Ireland
et al. 2007). Rainbow trout hatch earlier in response
to hypoxia and later in response to hyperoxia
(Latham and Just 1989).
Detecting and distinguishing among the diverse
patterns and mechanisms of hatching plasticity re-
quires assessment of changes in the timing of hatch-
ing, the rate and process of embryonic development,
and the phenotypes of hatchlings. A critical method-
ological issue is that definitions of developmental
stages strongly affect perceived variation in the de-
velopmental timing of hatching. Development is not
always synchronous across elements of morphology
and functional systems; thus, hatchlings that are at
equivalent stages by one criterion may be at different
stages by another criterion. For instance, red-eyed
treefrogs always hatch at Gosner (1960) Stage 23,
defined by the presence of bilateral external gills
and a full operculum. However, these animals vary
substantially in age, tail size, pigmentation, and the
development of their mouthparts, gut, and lungs
(Warkentin 1999). To identify such cases, ecologists
studying hatching must attend to details of develop-
ment. Traits that are changing during the period
when hatching occurs can serve as markers of devel-
Underlying the variation in the timing of hatching
are two kinds of mechanisms: (1) those that enable
phenotypic flexibility, separating the point in devel-
opment and/or the time when embryos can hatch
from when they must hatch; and (2) those that de-
termine the actual timing of hatching within this
period of competence to hatch, including sensory
and response mechanisms that link hatching to en-
vironmental cues and conditions. Flexible timing of
hatching depends on a variety of traits that contrib-
ute to survival and development both within and
outside the egg, as well as to the hatching process
(Warkentin 2007) (Fig. 1C). For instance, yolk limits
embryonic energy reserves and the structure of the
egg capsule affects oxygen supply. Hatchlings need
behaviors that were irrelevant in the egg and they
face a different osmoregulatory environment. The
process of hatching depends both on specific mech-
anisms, such as hatching enzymes or egg teeth, that
are unnecessary at any other time, as well as on more
general abilities, such as movement, that play a role
in other stages. Hatching becomes possible when re-
quirements for both the hatching process and life
outside the egg have developed, and will be limited
by the one that occurs last. Similarly, animals can
stay in the egg as long as all requirements for em-
bryonic survival are maintained, but as soon as one
is missing they must hatch or die. Thus, a variety of
traits, not all related to hatching itself, can limit
hatching plasticity, and these will differ among or-
ganisms. The opposing selection pressures that favor
plasticity in hatching will be focused on these limit-
Within the period of hatching plasticity, between
the onset and loss of hatching competence (Fig. 1C),
the actual timing of hatching may be determined
in different ways. Hatching could occur when some
developmental or physiological process reaches a
particular point. However, perhaps more often, mul-
tiple, partially correlated developmental processes
may contribute, with hatching becoming increasingly
likely as each proceeds (e.g., development or activity
of the hatching gland, elongation, increasing muscu-
lar strength, and activity, the oxygen demand to
supply ratio). Environmental effects on any or all
of the contributing processes could alter the timing
of hatching. Hatching may also be essentially a ‘‘de-
cision’’ based on information; i.e., it may depend on
a specific behavioral or physiological process that is
environmentally cued. The role of the cue may vary:
it could be (1) required, as in ‘‘ready and waiting’’
strategies [Fig. 1A(4)]; (2) the cue could initiate or
accelerate a hatching process that would eventually
occur without it, or the cueing requirement may
become increasingly permissive; or (3) the cue
could inhibit/delay hatching or increase the strin-
gency of some other requirement. In some species,
hatching may be elicited by any of multiple cues
(Warkentin and Caldwell 2009; Whittington and
Kearn 2011), or may require multiple conditions to
be met concurrently (Martin et al. 2011).
Attention to details of development may provide
clues to some of the traits and mechanisms that
contribute to plasticity in hatching (Warkentin
2007). For instance, traits that differ in their rate
or sequence ofdevelopmentbetween animals
at Leiden University on September 30, 2011
hatched at different ages or stages might either sub-
serve hatching plasticity or be sensitive to the change
in environment. Traits that show developmental
stasis while other traits change during a plastic
hatching period, particularly if they lack such a
period of stasis in related species that hatch at dif-
ferent stages, may be important for hatching compe-
tenceor forthe maintenance
development beyond the onset of competence.
Considering the evolved diversity in the timing of
hatching, the ecological importance of hatching as
a transition between life stages, and the widespread
plasticity in other life-stage transitions such as meta-
morphosis (reviewed in Werner and Gilliam 1984;
Benard 2004; Pechenik 2006), we might expect plas-
tic, cued hatching also to be widespread. Research on
ECH to date has focused on particular groups and
contexts, with different areas developing largely in-
dependently, in isolation from work on other groups
and contexts. There has been no systematic survey
and comparative analyses have been restricted in
scope (Martin 1999; Gomez-Mestre et al. 2008);
thus, there are undoubtedly large gaps in our under-
standing. Moreover, background assumptions of
fixed timing of hatching rarely have been rigorously
tested; we may know less about truly canalized
hatching than we do about hatching plasticity. To
set the symposium papers that follow in a larger
phylogenetic context and introduce the potential
breadth of ECH across animals, I offer a brief
survey illustrating the diversity of cued hatching.
There is, to my knowledge, no evidence for ECH
in the earliest-diverging metazoan lineages, cteno-
phores, sponges, and cnidarians. This may, however,
be more indicative of research effort than of biology,
as I am unaware of any studies testing for ECH in
these taxa. Within each of the three major clades of
bilaterian animals there are multiple lineages docu-
mented to have ECH in response to a wide range of
environmental variables, mediated by diverse types of
cue and mechanisms.
Much of the research on hatching plasticity in
Lophotrochozoa has focused on parasitic flatworms,
in which ECH is well-documented among all three
lineages: monogeneans (Whittington and Kearn
2011), trematodes (Sukhdeo and Sukhdeo 2004),
and cestodes (e.g, Mitterer 2008). Encapsulated em-
bryos of parasitic flatworms are hardier and more
tolerant of environmental variation than are newly
hatched larvae, whose survival necessitates specific
host resources at, or soon after, hatching. Embryos
respond to cues directly indicating, or associated
with, host availability and some species have a com-
plex, multimodal hierarchy of cues for hatching
(Whittington and Kearn 2011). The environmental
sensitivity of hatching has received much less atten-
tion in nonparasitic flatworms, but could be very
interesting in an evolutionary context.
Hatching plasticity has been examined in molluscs
in two contexts: as a response to food resources
for larvae and as a response to predators. Embryos
of two freshwater snails, Lymnaea stagnalis and
Helisoma trivolvis, slow development to half the
normal rate in response to cues from starved con-
specific juveniles, delaying hatching and the deple-
tion of yolk reserves (Voronezhskaya et al. 2004)
[Fig. 1A(3)]. The same species respond to hypoxia
by increasing embryonic rotation (and hence the
convection of oxygen) and by moving up oxygen
gradients within their large eggs (Goldberg et al.
2008). Both responses are meditated by the first
pair of neurons they develop (Kuang et al. 2002;
Voronezhskaya et al. 2004). In a nudibranch,
Phestilla sibogage, embryos hatch up to 60% prema-
turely within minutes when their gelatinous egg rib-
bons are physically damaged, scattering individual
capsules, as occurs during predation by crabs
(Strathmann et al. 2010) [Fig. 1B(3)]. This substan-
tially extends their period of obligate planktonic dis-
persal. Whelk (Nucella lamellosa) embryos delay
hatching in response to cues from predatory crabs
and isopods, and accelerate hatching in response to
cues from conspecific adults (Miner et al. 2010).
Among annelids, embryos of the polychaete
Platynereis dumerilii slow development and delay
hatching in response to chemical cues from starved
conspecifics (Voronezhskaya et al. 2008). In an egg-
brooding polychaete, Boccardia proboscidea, single
broods can include both planktotrophic, dispersive
hatch as juveniles after consuming nurse eggs and
(Gibson et al. 1999; Kamel et al. 2010). Mothers
determine the timing of hatching by tearing open
egg capsules, altering levels of sibling cannibalism
and the developmental stage and dispersive potential
of theiroffspringin response
(Oyarzun and Strathmann 2011).
larvae that typically
Among Ecdysozoa, ECH has been documented
in nematodes, a spider, crustaceans, and insects. In
many parasitic nematodes, hatching is stimulated by
cues emanating from or associated with the host, or
at Leiden University on September 30, 2011
inhibited by conditions unsuitable for infecting the
host (Perry 2002). For instance, among parasites of
plants, hatching both of cyst nematodes and of some
root-knot nematodes is cued by exudates from host
roots, and embryos can be sensitive to the species
and age of plants (Perry 1997; Perry and Wesemael
2008). Hatching of nematodes that are parasitic on
animals is often stimulated by physical conditions
in the host’s gut, which may be host-specific or spe-
cific to particular regions of the alimentary tract
(Perry 2002). For instance, in the mouse whipworm,
Trichuris muris, hatching depends on physical con-
tact of eggs with certain types of gut bacteria, as well
as on the correct, host-specific temperature (Hayes
et al. 2010).
Spitting spiders, Scytodes pallida, use sticky spit to
defend themselves. Carrying an egg sac impairs spit-
ting ability and egg-carrying females are preferred
prey of araneophagic jumping spiders, Portia labiata
(Li and Jackson 2003). Egg-brooding females induce
or directly cause their eggs to hatch early in response
to chemical cues from the jumping spiders, allowing
mothers to better protect themselves and their young
(Li 2002; Li and Jackson 2005).
Among crustaceans, timing of hatching varies with
direct and indirect cues indicating resource availabil-
ity for and risk to larvae. Timing of hatching may
be determined purely by embryos or be cued or
controlled by egg-brooding mothers. For instance,
larvae of the acorn barnacle, Semibalanus balanoides,
depend on the spring phytoplankton bloom for food.
Embryos are brooded within their mother’s mantle
cavity where they develop to hatching competence
and then wait, sometimes for months, for a
cue. Well-fed mothers produce an eicosanoid egg-
hatching pheromone, stimulating nauplii to hatch
with the spring phytoplankton bloom (Clare 1997).
In the tide-pool copepod Tigriopus japonicus, nauplii
normally hatch in 2–3 days. Under high conspecific
densities, egg-carrying mothers inhibit hatching of
developed, hatching-competent eggs for 24–48h,
during which time they may disperse to less-crowded
pools during high tides (Kahan et al. 1988). In sev-
eral freshwater species, including cladocerans, cope-
pods, clam shrimp, and fairy shrimp, chemical cues
from predators inhibit hatching of resting eggs
De Roeck et al. 2005). Cues from conspecific adults
can also inhibit hatching of resting eggs in several
species of fairy shrimp (Beladjal et al. 2007) and
there is extensive evidence that seasonal cues such
as photoperiod and temperature regulate hatching
(Gyllstro ¨m and Hansson 2004). Many crabs show
and Blaustein 2001;
highly synchronous, rhythmic hatching at times of
low risk of predation on larvae during diel, tidal,
and tidal-amplitude cycles (Christy 2011). The
hatching of decapods generally involves interactions
between embryos and egg-brooding mothers and
the role of each party varies among species (De
Vries and Forward 1991; Morgan 1995; Ziegler and
Much of the research on the hatching timing of
insects has focused on dormancy, in which embryos
undergo a period of arrested development in a state
of diapause orquiescence
Tauber et al. 1998; Kostal 2006). Arrest may occur
in early stages, so a period of development separates
the termination of dormancy from hatching, decou-
pling their timing [Fig. 1A(5)]. However, when dor-
mancy occurs late in embryonic development (E3 of
Andrewartha 1952), hatching and the end of dor-
mancy are tightly coupled [Fig. 1A(6)]. Studies of
the stimuli inducing hatching may not distinguish
these from cues that end dormancy and the extent
to which development and metabolism are slowed
or arrested while awaiting a cue to hatch varies.
Across species, insects use many seasonal cues
such as temperature, photoperiod, and moisture,
to hatch at favorable times; parasitic species of-
ten use cues provided by or associated with their
hosts (Andrewartha 1952; Tauber et al. 1998;
Kostal 2006). For example, the terrestrial eggs of a
dragonfly, Potomarcha congener, hatch upon flooding
(Miller 1992). Terrestrially laid eggs of Aedes mos-
quitoes require not only flooding to hatch, but also
the growth of bacteria which deplete oxygen in the
water; hatching can be inhibited by a high density of
conspecific larvae that consume the bacteria (Livdahl
et al. 1984; Livdahl and Edgerly 1987). Bot flies are
cutaneous parasites of vertebrates that respond to
cues from their hosts (Catts 1982). Human bot
flies, Dermatobia homins, glue their eggs to mosqui-
toes and other blood-feeding insects. Eggs become
hatching-competent in 5 days and can wait as long
as 20 days to hatch, which is a rapid response to a
sudden increase in temperature (Catts 1982; Cogley
and Cogley 1989).
Despite extensive research on the development of
echinoderms, including their phenotypic plasticity,
environmental effects on timing of hatching have re-
ceived little attention in this group. Recent work in-
dicates that low salinity can lead to delayed hatching
in a sand dollar, Echinarachinus parma. Embryos typ-
ically hatch as blastulae at 12h postfertilization;
under low salinity, they hatch as late as 26h, after
at Leiden University on September 30, 2011
gastrulation, as four-armed larvae (Armstrong and
Allen 2011). I am unaware of any research on ECH
in hemichordates or urochordates. There is, however,
extensive and widespread evidence for hatching plas-
ticity among vertebrates.
Several types of ECH have been documented
among fishes. Indeed fishes in general may require
an extrinsic or intrinsic stimulus to hatch, once
hatching competence is attained (Yamagami 1988).
Terrestrial eggs that hatch when flooded have
evolved multiple times (Martin 1999). In many
cases, hatching is cued by hypoxia (e.g, DiMichele
and Taylor 1980); in grunion mechanical tumbling
in waves stimulates hatching (Griem and Martin
2000; Martin et al. 2011). In some cases, the
timing of flooding and hypoxia is under parental
control (Ishimatsu and Graham 2011). Dissolved
oxygen can also affect the timing of hatching in
aquatic eggs of fishes; Latham and Just (1989) dem-
onstrated both accelerated hatching with hypoxia
and delayed hatching with hyperoxia in rainbow
trout. Moreover, hatching can be delayed by expo-
sure of normally aquatic fish eggs to air (Yamagami
1988), although several salmonids hatch prematurely
in response to impending exposure of eggs to air
(Wedekind and Mu ¨ller 2005). Annual fishes survive
seasonal drought as diapausing embryos at various
developmental stages. Diapause III, at a stage just
before hatching, may represent an evolutionary in-
tensification of the period of reduced metabolism
during delayed hatching of air-emerged embryos in
nonannual cyprinodonts (Wourms 1972). Some
fishes alter their timing of hatching in response to
cues from predators or pathogens. For instance, fat-
head minnows hatch early in response to chemical
cues from crayfish (Kusch and Chivers 2004) and
whitefish hatch early in response to bacterial infec-
tion of eggs (Wedekind 2002). Hatching at favorable
times in environmental cycles, as occurs in crusta-
ceans (Christy 2011) and monogeneans (Whittington
and Kearn 2011), may be common in fishes. For
example, the estuarine embryos of rainbow smelt
hatch synchronously shortly after dark, allowing fry
to wash out to sea while darkness offers protection
from visual predators (Bradbury et al. 2004).
Darkness also triggers hatching in the demersal
eggs of many tropical reef fishes, for which antipre-
dator benefits are also hypothesized (reviewed in
Asoh and Yoshikawa 2002).
Predator-cued shifts in the timing of hatching
were first discovered in
Moore 1993; Warkentin 1995) and hatching re-
sponses to biotic risks have received the most atten-
tion in that group. In many amphibians, embryos
hatch early in response to predators or pathogens
of eggs, and in a few species embryos delay hatching
in response to predators of larvae (reviewed in
Warkentin 2011). Amphibian embryos also respond
to physical environmental conditions. In multiple
lineages that have evolved terrestrial eggs, flooding
stimulates the hatching of aquatic larvae; dehydra-
tion of eggs can also accelerate hatching when eggs
are suspended above water
Tadpole-transporting parents may induce or mediate
hatching by physically manipulating eggs in some
poison-dart frogs (Brown et al. 2008, 2010).
ECH also occurs in reptiles in response to several
different risks and opportunities (Doody 2011,
Spencer and Janzen 2011). In Iberian rock lizards,
eggs hatch prematurely if infected with a fungal path-
ogen (Moreira and Barata 2005). Premature hatching
has been recorded in flooded Anolis sagrei eggs (Losos
et al. 2003) and anecdotal evidence suggests that phys-
ical disturbance, as by predators, may stimulate early
hatching in several lizards (Doody 2011). Eggs of
pig-nosed turtles, like terrestrially incubated fish
eggs, typically wait to hatch until flooded (Doody
2011) and there is evidence for synchronization of
hatching via responses to cues from siblings in several
turtles (Spencer and Janzen 2011). The vocalizations of
crocodilian embryos fine-tune hatching synchrony and
also stimulate mothers to help open the nest to free
hatchlings (Vergne et al. 2009). Synchronization of
hatching via acoustic interactions among siblings also
occurs in precocial birds, including waterfowl, and
quail (reviewed in Brua 2002). Depending on the
species, this may involve acceleration of hatching and
of some developmental processes by less developed
embryos, or retardation of hatching by more devel-
oped embryos (Vince 1969). Bird embryos may also
modulate hatching in respond to seasonal cues (Reed
and Clark 2011).
Hatching in mammals occurs at the blastocyst stage
and is necessary for embryos to implant in the uterine
wall. There is substantial variation in the period
between fertilization and implantation both among
and within species. About 100 species of mammals,
in seven orders, have delayed implantation (reviewed
in Renfree and Shaw 2000). Embryos develop to the
blastocyst stage and then stop or dramatically slow
development, waiting unhatched, sometimes for
months, until conditions in the uterus change, stimu-
lating hatching and implantation.
Factors affecting theevolutionof ECH
ECH is distributed across animal phylogeny in many,
diverse taxa. Timing of hatching varies in response
at Leiden University on September 30, 2011
to multiple environmental risks and opportunities,
mediated by a variety of cues and mechanisms.
Responses to similar factors occur in very distantly
related animals, suggesting convergent evolution,
although some may be ancient conserved traits.
Closely related species also differ in their responses
and patternsof hatching
Whittington and Kearn 2011). Our challenge now
is to integrate information on the timing of hatching
across taxa to better understand the diversity of pat-
terns. If we recognize that some level of plasticity—
including adaptive responses and susceptibility to
perturbation—is inherent in development (West
Eberhard 2003), and thus in hatching, logical next
questions are: what is the magnitude of this plasticity
and how is it structured in relation to different types
of environmental variation? Evolutionary theory on
phenotypic plasticity offers a starting point for inte-
grative and comparative analysis of the timing of
hatching, directing our attention to factors that
shape the diversity of plastic and fixed hatching
In general, selection favors plasticity in heteroge-
neous environments when there are trade-offs of fit-
ness across environmental conditions, cues that
predict conditions, and the benefits of phenotype–
environment matching outweigh costs of plasticity
(Via and Lande 1985; Moran 1992; Sultan and
Spencer 2002). Of the costs and limits that could
(DeWitt et al. 1998), the limits imposed by the reli-
ability of information and by time lags between
detection of and response to cues point to specific
aspects of development relevant to the evolution
For early life stages, far from reproductive matu-
rity and typically subject to high mortality, survival
is likely to be the most important component of
fitness, although development rate or other compo-
nents may mediate selection in some cases. When
environmental conditions predictably affect the like-
lihood of mortality within or outside the egg, so that
different hatching phenotypes are better under dif-
ferent conditions, there is an opportunity for adap-
tive plasticity to evolve. Many factors that affect the
survival of embryos or hatchlings also affect the
timing of hatching. These include physical conditions
that endanger eggs or hatched young, stage-specific
or stage-biased predators and pathogens, and hosts
or food resources required by hatchlings. They also
include conspecifics that either provide opportuni-
ties, such as parental care or safety in numbers, or
pose risks, such as competition for food.
of adaptive plasticity
In some cases, the timing of hatching is critical,
for instance for an embryo to escape from an attack-
ing egg-predator, an aquatic larva to avoid emerging
onto dry land, or a slow-moving parasite to make
contact with a highly mobile host. In other cases, the
developmental stage at hatching is more relevant, for
instance, to enable a hatchling to escape from pred-
ators it encounters, or in determining whether a
larva is competent to settle where it hatches or
enters an obligate period of planktonic dispersal.
Selective trade-offs may also exist across timing and
stage. For instance, selection by predators of eggs for
earlier hatching may oppose selection by predators of
larvae for hatching more developed. The relative
strength of selection on the timing of and develop-
mental stage at hatching should shape how hatching
plasticity is achieved, i.e., whether animals can hatch
across a broad developmental range or decrease their
rate of development at advanced embryonic stages,
extending the period of hatching competence. The
strength and shape of trade-offs and the nature of
environmental heterogeneity will also affect how
selection acts. For instance, when eggs are laid in a
habitat that only occasionally permits the survival of
larvae, selection to hatch at the right time is very
strong. More moderate heterogeneity in survival
rates, for instance due to variation in predation
risk to larvae, would impose weaker selection for
Given the number of abiotic and biotic environ-
mental variables that differentially affect mortality of
embryos and hatchlings, multiple selective factors
may contribute to each side of the trade-off that
favors hatching plasticity. These factors may combine
to increase the strength of selection for plasticity
within a population. Moreover, although their indi-
vidual importance may vary over time within line-
ages, their redundancy may contribute to the
maintenance of mechanisms that underlie flexibility
in the timing of hatching (Gomez-Mestre et al.
2008). Modularity of mechanisms contributing to
hatching plasticity can allow responses to particular
cues to change independently; these may be more
labile than the underlying capacity to hatch at dif-
ferent stages (Gomez-Mestre et al. 2008).
Environmental cues are critical for the evolution
of adaptive plasticity because they allow expression
of the right phenotype for the context. Thus, infor-
mation reliability limits how well organisms can
match phenotypes to conditions (DeWitt et al.
1998). Mismatches may arise from imperfect corre-
lations between cues and conditions or from errors
in assessment of cues. Sensory abilities, however,
change developmentally, and embryos can only
at Leiden University on September 30, 2011
respond to cues that they have developed the ability
to detect. This limits the potential onset of cued
hatching and the types of cues to which embryos
of different stages can respond. The earliest cued
hatching likely involves relatively simple mechanisms
while hatching of well-developed embryos may in-
volve more complex, multifaceted environmental as-
sessment. Selection may favor earlier development of
mechanisms that sense critical environmental vari-
ables. Alternatively, for species with parental care,
parents may sense and integrate cues, mediating
the response of embryos to variables they cannot
yet assess themselves.
The lag between the time a cue is detected and
when the organism responds to it can also limit the
value of plasticity (DeWitt et al. 1998). For hatching,
the magnitude of this lag depends on the hatching
mechanism, so variation in hatching mechanisms will
affect the environmental variables to which embryos
can respond as well as the types of information they
can use. For instance, a fast response is required for
embryos to escape from a sudden attack by a pred-
ator that consumes eggs rapidly. However, animals
with a slower hatching mechanism might benefit
from accelerated hatching in the context of a
slow-growing pathogen of eggs or indirect cues indi-
cating elevated risk of attack by a predator of eggs.
Similarly, lag-time limits on the value of host-cued
hatching are very different for a nematode embryo
waiting for the appropriate plant to grow nearby and
for a monogenean waiting for a fish to pause above
it. The diversity of hatching mechanisms will affect
how selection acts on hatching plasticity and the im-
portance of lag-time limits in different taxa. With
mechanisms for rapid hatching, selection may favor
precisely timed hatching and cued early hatching in
response to more diverse factors. Mechanisms that
allow faster hatching may also expand the contexts
in which delays in hatching could evolve by reducing
the duration of commitment to the hatching process
before hatching occurs. Similarly, strong selective
trade-offs and short notice of impending risks or
opportunities would favor a capacity to respond rap-
idly. Evolutionary changes in hatching mechanisms
will alter the range of factors to which embryos can
evolve adaptive responses, and affect the conditions
under which they can successfully develop.
Combining mechanistic and evolutionary perspec-
tives is necessary to understand ECH because devel-
opment changes how organisms interact with their
environments. Embryos have long been a focus for
studies of internal processes in animals isolated from
their environments. They also offer excellent oppor-
tunities for research on the adaptive responses of
organisms to their natural, variable environments.
Integrative and comparative research on the timing
of hatching will improve our understanding of em-
bryos as evolving, developing, responsive organisms.
I thank my symposium co-organizers, K. Martin
and R. Strathmann and all our symposium partici-
pants. My mentors and colleagues at STRI, especially
M. J. West-Eberhard, M. Ryan, W. Wcislo, and
J. Christy, have helped shape my thinking on ECH,
as have my collaborators in empirical studies of
hatching plasticity, especially I. Gomez-Mestre, J.
Vonesh, M.Caldwell, J. Touchon, and M. Hughey.
The manuscript was improved by comments from R.
Strathmann, I. Gomez-Mestre, T. Landberg, K. Cohen,
and an anonymous reviewer.
This symposium was supported by the Society for
Integrative and Comparative Biology and all of
its divisions,the National
HRD-0820175 to Boston University). The research
was supported by a Smithsonian Tropical Research
Institute Senior Fellowship, Boston University, and
the National Science Foundation (DEB-0716923).
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