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Integrative and Comparative Biology
Integrative and Comparative Biology, volume 53, number 4, pp. 713–722
doi:10.1093/icb/ict035
Society for Integrative and Comparative Biology
SYMPOSIUM
The Link Between Environmental Variation and Evolutionary Shifts
in Dormancy in Zooplankton
Matthew R. Walsh1
Department of Biology, University of Texas at Arlington, Arlington, TX 76019, USA
From the symposium ‘‘Phenotypic Plasticity and the Evolution of Gender’’ presented at the annual meeting of the Society
for Integrative and Comparative Biology, January 3–7, 2013 at San Francisco, California.
1
E-mail: [email protected]
Synopsis Sex and dormancy are intertwined in organisms that engage in asexual and sexual reproduction. The transition
between asexual and sexual reproduction typically results in a dormant stage that provides a mechanism for persisting
under harsh environmental conditions. For example, many zooplankton engage in sexual reproduction when environmental conditions deteriorate and produce resting eggs that remain viable for decades. It has long been assumed that
observed variation in the timing and magnitude of investment into a dormant stage among populations or species reflects
local environmental conditions. Yet, the importance of dormancy for the persistence of a given population can differ
dramatically among habitats (i.e., permanent vs. seasonal ponds). As a result, environmental conditions may exert
selection on the propensity for zooplankton to engage in sexual reproduction and enter dormancy in natural populations.
Here, I highlight a growing body of research illustrating an important link between environmental conditions and
divergent reproductive strategies in zooplankton. I specifically: (1) review the environmental cues that initiate a transition
between asexual and sexual reproduction in zooplankton and (2) describe recent work demonstrating an evolutionary
consequence of ecological selective pressures, such as predation and habitat predictability, on variation in the extent to
which organisms engage in sex and enter dormancy. Such results have implications for the genetics and ecology of these
organisms.
Introduction
Spatial and temporal environmental variation is a
ubiquitous feature of natural systems. Severe changes
in environmental conditions can influence rates of
survival and reproduction. As a result, many taxa
exhibit a life-history stage, such as diapause and dormancy, that enables organisms to avoid unfavorable
conditions (Roff 1992; Stearns 1992). There are clear
fitness costs and benefits associated with such traits.
On the one hand, the dormant stage allows an individual to persist during harsh periods (Cáceres 1997;
Caceres and Tessier 2004). Conversely, the dormant
life-history stage reduces opportunities for reproduction and growth (Ellner 1997; Shefferson et al. 2003).
As a result, key decisions regarding when to enter
dormancy and how much to invest in the dormant
stage are likely under strong selection in natural
populations.
In organisms that are capable of asexual and
sexual reproduction (i.e., facultative parthenogens),
there is a tight association between the sexual lifehistory stage and the onset of dormancy (Bell 1982;
Tessier and Caceres 2004). For example, many species of zooplankton (e.g., Daphnia sp.) reproduce
asexually until environmental conditions change
and specific cues promote the transition to sexual
reproduction. The sexual stage is characterized by
the production of males that reproduce sexually
with females to produce weather-resistant resting
eggs (ephippia) (Gyllstrom and Hansson 2004).
However, many species of zooplankton, and organisms in general, are found in a diversity of habitats
that differ tremendously in their severity. Such
examples may include variation in permanence of
the habitat (temporary vs. permanent ponds), seasonal predation risk, or productivity (i.e., Campillo
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714
et al. 2011; Walsh and Post 2012). This variation
is important because the benefits associated with
dormancy may vary with local environmental conditions. For instance, dormancy may be of greater
value in ephemeral habitats than at permanent
locales. It is even plausible that dormancy may be
required very infrequently in some habitats (Tessier
and Caceres 2004). If the decision to engage in sex
and enter dormancy is heritable, it then follows logically that local environmental conditions may, in
turn, select for evolutionary shifts in dormancy
patterns.
Evolutionary theory makes predictions regarding
the conditions that should select for changes in
either the induction or investment in sex and dormancy. On the one hand, the decision to engage in
sexual reproduction and enter dormancy represents a
form of phenotypic plasticity. Plasticity is generally
favored when the environment is variable but predictable (Levins 1968; Lively 1986; Scheiner 1993;
Schlichting and Pigliucci 1998; Alpert and Simms
2002). More specifically, theory predicts that the initiation of the dormant stage is favored by reliable
environmental cue(s) that indicate a future change
in the environment that has negative consequences
for the fitness of an organism (Hairston and Munns
1984). Populations that experience predictable
changes in an important feature of the environment
(i.e., predation, seasonality) will be expected to respond strongly to cues that forecast this change in
environmental conditions and engage in sex (and
thereby enter dormancy) to a much extent than populations that experience an unvarying environment
or unpredictable variation. An alternative body of
theory considers the factors that determine allocation
toward dormancy and predict that the total investment in dormancy depends upon the change in fitness between the active and dormant life-history
stages (Cohen 1970; Taylor 1980). Enhanced allocation toward sex and dormancy is favored when the
fitness of the active stage is lower than that of the
dormant stage. Although much research has explored
the cues that initiate the induction of sexual reproduction and, thereby, dormancy (i.e., Hobaek and
Larsson 1990; Kleiven et al. 1992; Spaak and
Boersma 2001; Deng et al. 2010), subsequent exploration of a link between local environmental conditions and evolutionary shifts in dormancy patterns,
especially in zooplankton, has lagged behind (but see
Dedryver et al. 2001).
Here, I review a growing body of evidence illustrating significant genetic variation in dormancy
strategies in zooplankton in freshwater environments.
Zooplankton, such as Daphnia spp., have long served
M. R. Walsh
as model organisms to address outstanding questions
in ecology and evolutionary biology (Stollewerk
2010; Lampert 2011; Miner et al. 2012) and recent
research focused on natural populations of zooplankton has significantly advanced our understanding of
the connection between environmental variation and
evolutionary shifts in dormant life-history stages.
This work has demonstrated that the decision to
engage in sexual reproduction (and initiate dormancy) can vary significantly among natural populations and is subject to strong ecologically-mediated
selection. I first review prior work that has evaluated
the environmental cues that initiate the transition
between asexual and sexual reproduction. Such
work provides information on the factors that
induce the dormant stage and may, thereby, exert
selection on investment in dormancy in natural populations. Second, I describe work that has evaluated
natural populations for genetic divergence in the induction of sexual reproduction and dormancy.
Finally, I synthesize what we now know about patterns of investment in dormancy and identify pertinent future directions for research.
Environmental cues that induce sexual
reproduction
The environmental cues that can initiate sex and
dormancy in zooplankton have received much attention (Gyllstrom and Hansson 2004). Researchers typically manipulate environmental factors that are
representative of natural conditions and then quantify investment in dormancy by measuring the production of males and/or sexual females. A majority
of these efforts have focused on cladocerans. To
summarize current understanding, I searched the literature for studies on cladocerans that examined the
cues that can induce sex and diapause in a laboratory
setting. This extensive, but likely not exhaustive
review yielded revealed 31 studies spanning 14 species (Table 1). Below I describe the trends that are
apparent from this work.
Which cues induce sex?
This body of work has shown that environmental
variables, including chemical cues from predators
(fish and invertebrate predators), population density,
water temperature, photoperiod, and availability and
quality of resource can cause increases in the formation of resting eggs (ephippia) and/or production of
males (Table 1). Specifically, increases in population
density, decreases in food levels, food quality, or
photoperiod, and the presence of cues emanating
from predators frequently, but not always, initiate
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Environmental variation and evolutionary shifts in zooplankton
Table 1 Studies exploring the environmental cues that induce the production of males and/or ephippia in cladocerans
Species
Cue
Response
Inter.
References
Bosmina longirostris
T R PH
Higher temp increased ephippia production
N
Bhajan and Hynes (1972)
Daphnia galeata
RQ
Lower quality algae induced ephippia formation
N/A
Koch et al. (2009)
Daphnia galeata
FP
Predator cue decreased ephippia production (for some
crosses)
N/A
Spaak and Boersma (2001)
Daphnia carinata
CY
Cyanobacteria decreased ephippia production
N/A
Deng et al. (2010)
Daphnia carinata
IP
Predator cue decreased ephippia production
N/A
Barry (2000)
Daphnia cucullata
CC
No response
N/A
Lurling et al. (2003)
Daphnia
longicephella
IP
No response
N/A
Barry (2000)
Daphnia longispina
FP
Predator cue increased ephippia production
N/A
Slusarczyk et al. (2012)
Daphnia lumholtzi
FP
Predator cue increased ephippia production
N/A
Dzialowski et al. (2003)
Daphnia lumholtzi
IP
No response
N/A
Dzialowski et al. (2003)
Daphnia magna
FP
Predator cue increased ephippia production
N/A
Mikulski and Pijanowska (2009)
Daphnia magna
FP PH
Predator cue increased ephippia production in light only
Y
Slusarczyk et al. (2005)
Daphnia magna
FP R
Predator cue increase ephippia production but stronger
response under low food
Y
Slusarczyk (2001)
Daphnia magna
FP
Predator cue increased ephippia production
N/A
Slusarczyk et al. (2012),
Pijanowska and Stolpe (1996)
Daphnia magna
R, D, PH
Low photoperiod, reduced food, increased density increased ephippia production
N/A
Carvalho and Hughes (1983)
Daphnia magna
FP
Predator cue increased ephippia production
N/A
Slusarczyk (1995)
Daphnia magna
FP T
Predator cue combined with decreasing temperatures increased ephippia production
Y
Slusarczyk and Rybicka (2011)
Daphnia magna
FP AC
Production of ephippia required predator and alarm cues;
males produced with either cue
Y
Slusarczyk (1999)
Daphnia magna
R CC PH
Crowding cue, short daylength increased male offspring
production
N/A
Hobaek and Larsson (1990)
Daphnia magna
CC PH R
Crowding, food limitation, and short photoperiod induced
ephippia and males
Y
Kleiven et al. (1992)
Daphnia magna
RD
Food limitation and crowding were needed to induce
males and ephippia production
Y
Olmstead and LeBlanc (2001)
Daphnia magna
T, PH
Low temperature, decreased photoperiod-induced male
production
Y
Korpelainen (1986)
Daphnia magna
D, R, T, PH
High density, short photoperiods increased ephippia
production
N/A
Bunner and Halcrow (1977)
Daphnia magna
D
High density increased ephippia production (but not male
production)
N/A
Yampolsky (1992)
Daphnia magna
CC Par
Crowding-induced sex; parasites did not significantly alter
sex investment
Y
Duncan et al. (2009)
Daphnia mendotae
T
No response
N/A
Bernot et al. (2006)
Daphnia pulex
CC
Crowding increased ephippia production
N/A
Lurling et al. (2003),
Fitzsimmons and Innes (2006)
Daphnia pulex
CY
Cyanobacteria increased ephippia production
N/A
Deng et al. (2010), Lauren et al.
(1997)
Daphnia pulex
D, PH
Short photoperiod, increased density induces ephippia
production
Y
Stross and Hill (1965)
Daphnia pulex
RQ
Low-quality algae induced ephippia formation
N/A
Koch et al. (2009)
Daphnia pulicaria
T
High temperature increased ephippia production
N/A
Bernot et al. (2006)
Daphnia pulicaria
FP
Predator cue increased ephippia production
N/A
Slusarczyk et al. (2012)
(continued)
716
M. R. Walsh
Table 1 Continued
Species
Cue
Response
Inter.
References
Daphniopsis
ephemeralis
T
Low temperature increased males and ephippia
production
N/A
Stirling and McQueen (1986)
Moina brachiata
CC
Crowding increased ephippia production
N/A
Zadereev and Lopatina (2007)
Moina macrocopa
R
Low food increased males and ephippia production
N/A
D’Abramo (1980)
Moina macrocopa
CC
Crowding increased ephippia production
N/A
Zadereev and Lopatina (2007)
Moina micrura
FP
No response
N/A
Santangelo et al. (2010)
Cues: T, temperature; R, resource level; RQ, resource quality; PH, photoperiod; CY, cyanobacteria; D, density; CC, crowding cues; FP,
fish predator; IP, invertebrate predator; Par, parasite. The interaction (inter.) column indicates whether the induction of sex depended
upon multiple cues.
the transition between asexual and sexual reproduction (Table 1). Previous work has also shown that
increases (i.e., Slusarczyk and Rybicka 2011) and
decreases (i.e., Korpelainen 1986) in temperature
can induce sexual reproduction. All of these cues
have potential ecological relevance to natural populations. For instance, increased crowding or a reduction in availability of food may signal a decline in
conditions and favor the transition to dormancy.
A decline in photoperiod may indicate the onset
of autumn/winter when a dormant stage is likely
favored. Fish are also well known to negatively
impact the abundances of zooplankton (Pace et al.
1999; Post et al. 2008) and thus the transition to
sexual reproduction in the presence of fish is logical.
Pijanowska and Stolpe (1996) specifically hypothesized that the formation of resting eggs may result
in a higher fitness than does parthenogenetic reproduction when predation pressure is high, a response
that is supported by several experimental results
(Table 1). Depending upon the thermal tolerances
of specific species of cladocerans and the seasonal
variation observed in a given environment, the initiation of sex and dormancy could potentially be
advantageous under either high or low temperatures.
Interactions among cues
In many studies, researchers used factorial designs
to explore the interactive effects of multiple environmental cues on the initiation of the dormant stage.
Such work frequently found that investment in dormancy depends upon the combined effects of several
cues (Table 1). For example, Slusarczyk (2001) showed
that cues from predators initiated the production of
ephippia in Daphnia magna, but the production of
ephippia was even higher when resources were limiting. Work has shown that these interactions can involve an interplay between cues from predators and a
variety of other environmental variables (food levels,
photoperiod, and temperature) as well as interactions
among environmental variables that are likely to
covary in lakes (temperature, photoperiod, density,
and availability of food). In addition to influencing
overall investment in dormancy, the interactive effects
of multiple environmental variables can influence
the induction of sex and dormancy (Table 1). Kleiven
et al. (1992) showed that a combination of crowding,
limitation of food, and short photoperiod were all
required to induce sexual reproduction in D. magna.
Interestingly, the transition to sexual reproduction was
sensitive to multiple environmental cues in all but one
study that utilized a factorial design (Table 1). This
indicates that studies utilizing a single environmental
cue may provide limited insight into the factors that
promote the transition to the dormant stage in natural
populations.
Evolutionary shifts in dormancy
strategies
The next key step in the exploration of dormancy
patterns in zooplankton is to determine if/how local
environmental conditions exert selection and facilitate
genetic changes in allocation toward dormancy. Below
I describe research illustrating: (1) genetic variation in
the induction or investment in dormancy, (2) divergence in dormancy patterns in the field, and (3) evolutionary shifts in dormancy strategies.
Genetic variation in sexual investment
Genetic variation, along with selection, provides the
raw materials for evolutionary processes. Early work
that dealt with the potential link between environmental conditions and selection on the dormant
stage revealed significant genetic variation in the production of males and ephippia among clones of
facultative parthenogens within the same population
(Loaring and Hebert 1981; Ferrari and Hebert 1982;
Carvalho and Hughes 1983; Korpelainen 1986;
Ruvinsky et al. 1986; Yampolsky 1992; Deng 1996;
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Environmental variation and evolutionary shifts in zooplankton
Tessier and Caceres 2004; Fitzsimmons and Innes
2006). For instance, Yampolsky (1992) quantified
the production of males and ephippia of several
clones of D. magna across a range of population
densities. Clonal investment in sex and dormancy
differed strongly as a function of increasing population density. A similar approach revealed significant
genetic variation in the induction of sex in response
to manipulations of photoperiod and availability of
food (Deng 1996). The results of this work imply
that a change in environmental conditions or variation among lakes in environmental conditions has
the potential to drive evolutionary shifts in allocation
toward the dormant life-history stage.
Field-based evidence for divergence in sexual
reproduction
Daphnia across a climatic gradient
Ferrari and Hebert (1982) explored multiple populations of D. magna for variation in the induction of
sexual reproduction and the onset of dormancy.
They compared the production of males and resting
eggs in response to a change in photoperiod between
a population from the arctic versus one from the
UK. The authors found that Daphnia from the
arctic responded to a decline in photoperiod by producing males and then resting eggs while the clones
from the UK did not engage in sex when photoperiod was reduced. Since the latter populations were
reared in the laboratory, the divergent responses to
a change in photoperiod are likely genetic in origin.
More importantly, the divergent responses to a
decline in photoperiod suggest that photoperiod
forecasts worsening environmental conditions for
the arctic population (more so than for the population from the UK) and that the arctic population
adaptively transitions between asexual and sexual
reproduction when photoperiod declines.
Several studies have examined populations of zooplankton that differ in their environmental conditions
or that experience a change in the environmental conditions for variation in sexual reproduction and dormancy in the field (Innes 1997; Caceres and Tessier
2004; Schroder et al. 2007; Gilbert and Dieguez 2010;
see also Hairston and Walton 1986; Hairston and Van
Brunt 1994). In one such study, Innes (1997) showed
that Daphnia pulex from temporary lakes are characterized by an earlier transition to sexual reproduction
than Daphnia from permanent bodies of water. Similar
studies have shown that rotifers from temporary habitats are characterized by an early onset or higher investment in dormancy (Schroder et al. 2007; Gilbert
and Dieguez 2010). Such results imply a link between
habitat stability and/or predictability and selection for
the initiation of dormancy (see also Hairston and Van
Brunt 1994). In a similar study, Caceres and Tessier
(2004) quantified the occurrence of sexual reproduction in Daphnia pulicaria across several lakes varying in
size, resources, and risk of predation. In general, they
found that populations of Daphnia that were exposed
to the greatest risk of predation and exhibited large
seasonal declines in abundance (presumably from predation) were characterized by high investment in dormancy. This work indicates that the timing and overall
investment in dormancy depend upon specific ecological conditions. However, the extent to which observed
variation in dormancy reflects genetic versus environmental sources was not established.
Tessier and Caceres (2004) examined populations of
D. pulicaria across a gradient in resources and risk of
predation for variation in the production of males
and resting eggs. During the summer, Daphnia are
often exposed to intense predation by fish. To avoid
predation, Daphnia migrate to cold, deep refuges at
the bottoms of lakes (Leibold and Tessier 1997).
However, the lakes included in this study varied
greatly in the size of these refuges, which, in turn,
leads to variation in risk of predation; larger refuges
correlate with lower intensity of predation. In this
study, the authors reared nine populations of
Daphnia across photoperiods that mimic the differences between spring and summer and exposed all
individuals to water conditioned by high densities of
Daphnia engaging in frequent sexual reproduction.
Such an approach revealed population-level differences in the induction of sex between spring and
summer as well as overall differences in allocation
toward dormancy. In general, agreement with
theory (Cohen 1970; Taylor 1980), populations characterized by greater increases in risk of predation
frequently, but not always, exhibited a higher production of males and sexual resting eggs.
Evolutionary changes in sexual investment
Intermittent versus consistent risk of predation
Research that encompasses a variety of ecological
contexts has provided evidence for a genetic basis
for differences in the induction of sex and dormancy
and/or overall investment in dormancy in natural
populations.
Walsh and Post (2012) evaluated patterns of sexual
reproduction in Daphnia ambigua from populations
in which the dominant fish predator either does
or does not migrate between marine and freshwater
environments for the purposes of spawning.
Gradient in risk of predation
718
Anadromous alewife (Alosa pseudoharengus) migrate
into lakes each spring to spawn and their offspring
spend several months each year feeding on zooplankton in lakes before returning to the ocean. In contrast,
landlocked alewives are permanent freshwater residents and prey upon zooplankton in lakes year
round (Brooks and Dodson 1965; Post et al. 2008).
As a result, Daphnia are abundant in ‘‘anadromous
lakes’’ during the spring but are eliminated by juvenile
alewife predation in early summer (Post et al. 2008).
Daphnia in ‘‘landlocked lakes’’ are consistently found
at low abundances due to the permanent presence of
alewife. These populations thus differ strongly in the
predictability of predation pressure. Daphnia from
lakes with anadromous alewife experience consistent,
predictable increases in predation each year, while predation pressure is permanently strong in lakes with
landlocked alewife. To evaluate the influence of the
predictability of alewives’ presence on the transition
to sexual reproduction in Daphnia, Walsh and Post
(2012) reared Daphnia from lakes with anadromous
and landlocked alewife in the presence and absence
of alewife chemical cues. The results showed that
Daphnia from lakes with anadromous populations responded to predator cues by significantly increasing
the production of males, while Daphnia from lakes
with landlocked alewife exhibited minor differences
in sexual activity between treatments that either did
or did not contain cues from predators. Such results
are consistent with classic plasticity theory (i.e.,
Hairston and Munns 1984) and indicate a link between
variation in a predatory fish and evolutionary shifts in
the extent to which Daphnia will engage in sex and
enter dormancy.
Variation in sex as a function of body size
Slusarczyk et al. (2012) hypothesized that avoidance
of predators is one of the main functions of dormancy in zooplankton. Since larger zooplankton
are likely more susceptible to visually oriented predators, such as fish, they predicted that larger species
of zooplankton would exhibit a greater propensity to
engage in sex and transition to a dormant life-history
stage in the presence of predators. They tested this
prediction by rearing three species of Daphnia
(D. magna, D. pulicaria, Daphnia longispina) that
vary in body size in the presence and absence of
fish. The results showed that predator cues induced
the transition to sexual reproduction in all three species, but the magnitude of the response varied across
species; there was a positive relationship between
body size and the induction of sexual reproduction
(and dormancy) as the largest species (D. magna)
initiated sex with the highest frequency. This study
M. R. Walsh
derived genotypes from the same lake and performed
the experiment in a common garden setting. The
results thus reflect genetic variation among species
and support the hypothesis that size-selective predation may drive evolutionary shifts in the ‘‘decision’’
by zooplankton to enter dormancy.
Temporary versus permanent ponds
Researchers have used populations or species of zooplankton from temporary versus permanent aquatic
habitats to quantify genetically-based divergence in
dormancy patterns. In one such study, Deng (1997)
leveraged known differences in the distribution of
two zooplanktonic species as a means of exploring
patterns of sexual reproduction and diapause production. Daphnia pulicaria and D. pulex are closely
related species typically found in divergent habitats.
Daphnia pulex commonly inhabit ponds that predictably fill with water in the spring and subsequently
dry-up in summer. In contrast, D. pulicaria inhabit
permanent bodies of water and their populations
usually decline in autumn. To quantify variation in
patterns of sexual reproduction and dormancy, Deng
(1997) reared each species of Daphnia under photoperiods that mimic summer (long-day photoperiod)
versus autumn (short-day photoperiod) conditions.
Sex was induced in D. pulex by long-day photoperiods, while the opposite trend was observed for D.
pulicaria (i.e., short-day photoperiod-induced sex).
Such results indicate that each species is adapted to
habitat-specific environmental cues. Since D. pulex
inhabit temporary environments that dry each
summer, the ability to recognize cues that forecast
the onset of summer is likely to be particularly important for this species.
Using a similar framework of natural populations,
Campillo et al. (2011) explored dormancy patterns in
a rotifer, Brachionus plicatilis, across six populations
that differ in permanence of habitat in Spain. These
aquatic habitats varied from highly ephemeral to permanent. In concordance with the results from prior
field studies (Schroder et al. 2007; Gilbert and
Dieguez 2010), the authors showed that populations
from temporary habitats invested more heavily in the
production of males and resting eggs than did populations from more permanent environments (see
also Deng 1997).
The generality of these results from natural populations (Deng 1997; Campillo et al. 2011) is further
supported by recent studies of experimental evolution performed in the laboratory. Smith and Snell
(2012) evaluated evolutionary changes in patterns
of sexual reproduction and dormancy in laboratory
populations of a rotifer that consistently experienced
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Environmental variation and evolutionary shifts in zooplankton
very stable conditions (i.e., ‘‘permanent habitats’’)
versus treatments that were ‘‘temporary’’ and were
frequently restarted with new offspring from diapausing eggs. This experiment showed that less
stable conditions in the laboratory selected for the
evolution of increased investment in sex and dormancy. Similar experiments on laboratory selection
illustrated a link between spatial environmental variability and increased allocation toward sex in rotifers (Becks and Agrawal 2010, 2012). Collectively, the
studies both of natural and laboratory populations
indicate that variation in the permanence of habitats
may act as a particularly strong agent of selection on
the ‘‘decision’’ by zooplankton whether or not to
engage in sex and enter dormancy.
Synthesis and directions for future
research
A growing body of research has illustrated important
connections between variation in ecological parameters and divergence in dormancy patterns in zooplankton. Ecological variation in risk of predation (Tessier
and Caceres 2004; Walsh and Post 2012) and permanence of habitats (Ferrari and Hebert 1982; Campillo
et al. 2011; Smith and Snell 2012) appear to exert
strong selective pressures on dormancy strategies.
Such work confirms the long-held assumption of
an adaptive value for dormancy in zooplankton, but,
more importantly, begins to establish the factors that
drive evolutionary shifts in dormancy patterns (i.e.,
Tessier and Caceres 2004; Walsh and Post 2012).
Given that transitions between asexual and sexual reproduction and associated connections with dormancy
are prevalent in a diverse array of organisms, the work
described in this article has implications that extend
beyond aquatic habitats. In general, the evolution of
plasticity associated with diapause and dormancy is a
topic that has largely been ignored by empiricists. This
is surprising given that variation in sexual reproduction and dormancy in zooplankton is a topic that is
seemingly well connected to areas of research, such as
phenotypic plasticity, bet-hedging, and the evolution
of life history that have received much attention. As a
result, I believe there are several pertinent directions
for future research.
Discrepancy between research on environmental
cues and evolutionary responses to
environmental cues
The majority of research on the transition between
asexual and sexual reproduction in zooplankton has
focused on the cues that induce sex and dormancy.
For instance, 430 studies have quantified the cues
that induce sexual reproduction (Table 1), but only
a few studies provide strong evidence for genetic
changes in dormancy (e.g., Ferrari and Hebert
1982; Tessier and Caceres 2004; Slusarczyk et al.
2012; Walsh and Post 2012). Research now needs
to place a greater emphasis on exploring the conditions that favor evolutionary shifts in dormancy patterns. Past research has shown that variation in
predation and in the stability of the habitat is associated with divergence in patterns of sexual reproduction and dormancy (Innes 1997; Caceres and
Tessier 2004; Tessier and Caceres 2004; Walsh and
Post 2012). However, it is also clear that a diverse
array of ecological variables can induce the onset of
sexual reproduction (Table 1), although the extent to
which variation in temperature, competition, or
availability of resources molds evolutionary changes
in dormancy patterns are unknown. One possibility
is for researchers to examine gradients of latitudinal
variation in temperature and seasonality in search of
trends in the induction of sex and dormancy (Ferrari
and Hebert 1982; see also Mousseau and Roff 1989).
Adaptive variation in gender specialization?
Interestingly, several laboratory studies have provided
evidence that genotypes specialize when engaging in
sex by producing males ‘‘or’’ sexual females but not
(necessarily) both (Innes and Dunbrack 1993; Innes
and Singleton 2000; Tessier and Caceres 2004; Walsh
and Post 2012). There is also evidence that these
‘‘gender specialists’’ transition to sex under contrasting environmental conditions. Tessier and Caceres
(2004) reared populations of Daphnia under photoperiods that mimicked either ‘‘spring’’ or ‘‘summer’’
conditions. They found that ‘‘male specialists’’ engaged in sex under spring conditions but reduced
sexual investment when exposed to photoperiods indicative of summer. The opposite trends were observed for genotypes that specialize in sexual
function in females. The consistent association between variation in an environmental cue and the
production of a specific sexual function (males or
sexual females) implies that gender specialization is
potentially adaptive. Yet, many questions regarding
the importance of gender specialization are entirely
unexplored. Does variation in environmental factors
select for changes in gender specialization and, if
so, which variables are key to shifts in gender specialization? Does gender specialization covary, either
positively or negatively, with sexual investment? Is
gender specialization common across taxa? Answers
to such questions will resolve an additional layer of
complexity in the association between environmental
variation and sex.
720
Sex, genetics, and the ecology of organisms
Variation in dormancy patterns may have ecological
and evolutionary ramifications. For example, populations that are characterized by minimal investment
in sex and dormancy may experience declines in
clonal diversity and genetic variation, and possibly
experience increases in the accumulation of deleterious mutations (Lynch 1984; Tessier et al. 1992;
Lynch et al. 1993). A lower propensity to engage in
sex and lower amounts of genetic variation may, in
turn, limit the capacity of some populations to respond to future changes in the environment (Tessier
and Caceres 2004). From an ecological perspective,
variation in sex and dormancy may differentially influence the population dynamics of zooplankton.
The transition to sexual reproduction reduces the
proportion of individuals that are reproducing asexually and will presumably lower rates of population
growth. This pathway from sex to population growth
is especially important in Daphnia sp., due to their
important roles as grazers on phytoplankton and as
food for larger taxa (Carpenter et al. 1987, 1992;
Elser et al. 1988). At the very least, variation in sex
and dormancy patterns provides the opportunity to
explore links between the ecology of organisms, selection for phenotypic plasticity, and the genetics of
populations. This includes an additional means
whereby researchers can explore how intraspecific
variation modifies the properties of populations
and communities (e.g., Schoener 2011).
Acknowledgments
I thank two reviewers for constructive comments.
I also thank Jan Leonard for organizing the symposium on ‘‘Phenotypic plasticity and gender roles’’
that lead to this article.
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