ADAPTIVE MATERNAL ADJUSTMENTS OF OFFSPRING SIZE IN RESPONSE TO CONSPECIFIC DENSITY IN TWO POPULATIONS OF THE LEAST KILLIFISH, HETERANDRIA FORMOSA
←
→
Page content transcription
If your browser does not render page correctly, please read the page content below
B R I E F C O M M U N I C AT I O N
doi:10.1111/j.1558-5646.2009.00631.x
ADAPTIVE MATERNAL ADJUSTMENTS
OF OFFSPRING SIZE IN RESPONSE TO
CONSPECIFIC DENSITY IN TWO POPULATIONS
OF THE LEAST KILLIFISH, HETERANDRIA
FORMOSA
Jeff Leips,1,2 Jean M. L. Richardson,3,4 F. Helen Rodd,1,3,5 and Joseph Travis1
1
Department of Biological Science, Florida State University, Tallahassee, Florida 32306
2
Department of Biological Sciences, University of Maryland Baltimore County, Baltimore, Maryland 21250
3
Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Ontario M5S 3G5, Canada
4
Department of Biological Sciences, Brock University, St. Catharines, L2S 3A1, Canada
5
E-mail: helen.rodd@utoronto.ca
Received August 26, 2008
Accepted December 11, 2008
Given a trade-off between offspring size and number and an advantage to large size in competition, theory predicts that the
offspring size that maximizes maternal fitness will vary with the level of competition that offspring experience. Where the
strength of competition varies, selection should favor females that can adjust their offspring size to match the offspring’s expected
competitive environment. We looked for such phenotypically plastic maternal effects in the least killifish, Heterandria formosa, a
livebearing, matrotrophic species. Long-term field observations on this species have revealed that some populations experience
relatively constant, low densities, whereas other populations experience more variable, higher densities. We compared sizes of
offspring born to females exposed during brood development to either low or high experimental densities, keeping the per
capita food ration constant. We examined plastic responses to density for females from one population that experiences high and
variable densities and another that experiences low and less-variable densities. We found that, as predicted, female H. formosa
produced larger offspring at the higher density. Unexpectedly, we found similar patterns of plasticity in response to density for
females from both populations, suggesting that this response is evolutionarily conserved in this species.
KEY WORDS: Competition, life-history strategies, maternal effects, optimal offspring size, phenotypic plasticity.
Environmental conditions experienced by offspring during pre- mothers respond to environmental challenges by manipulating
and postnatal development can have dramatic effects on their the phenotype of individual offspring to enhance their fitness in
fitness (e.g., Clutton-Brock 1991; Mousseau and Fox 1998; that environment. These adaptive maternal effects include adjust-
Holbrook and Schal 2004). An important source of these effects ments of nutrient provisioning, hormones (Benton et al. 2005;
is the maternal environment; stressful conditions experienced by Meylan and Clobert 2005), and agents that enhance resistance to
the female parent can reduce offspring fitness (McCormick 1998; disease (Spitzer 2004).
Jann and Ward 1999; Naguib et al. 2006) but, in certain cases, The initial size of free-living offspring has been a focal trait
for studies of adaptive maternal effects because, in a broad range
All authors contributed equally in this article. of taxa, the environment experienced by the dam affects size of
C 2009 The Author(s). Journal compilation
C 2009 The Society for the Study of Evolution.
1341 Evolution 63-5: 1341–1347B R I E F C O M M U N I C AT I O N
eggs or size at birth (reviewed in Bernardo 1996; Mousseau and in offspring continuously in response to environmental circum-
Fox 1998) and larger offspring sizes are associated with higher stances. Long-term field studies of H. formosa populations impli-
early-age survivorship (e.g., Henrich 1988; Bridges and Heppell cate intraspecific competition as an important determinant of indi-
1996; Persson et al. 1996; Heath and Blouw 1998; Magnhagen and vidual fitness that varies in strength among populations and even
Heibo 2001; Sakwinska 2004, reviewed in Azevedo et al. 1997; across time within some populations (Richardson et al. 2006).
Allen et al. 2008, but see Gomez 2004). Even when paternal Conspecific density can be extremely high but vary seasonally
genotype influences size at hatching or size at birth, maternal in some populations, whereas other populations have a chron-
control is the predominant influence (e.g., Travis 1981; Travis ically low density with much less seasonal fluctuation (Leips
et al. 1987). and Travis 1999; Soucy and Travis 2003). Adults and juveniles,
Perhaps the greatest advantage of an increased size comes including newborn offspring, are found in the same microhabi-
from an enhanced ability to compete with conspecifics (e.g., tats (Leips and Travis 1999; Richardson et al. 2006), so mater-
Stanton 1984; Marshall et al. 2006). When competition among ju- nal experience can usually predict the density that offspring will
veniles for resources is intense, a small increase in size at birth can experience.
improve expected fitness (Wilbur and Collins 1973; Parker and Here we ask (1) Do female H. formosa increase the size
Begon 1986; Pen et al. 1993; Both et al. 1999; Benton et al. 2005; of their offspring, at the cost of fewer offspring per brood, in
Allen et al. 2008; Bashey 2008). The importance of offspring size response to greater conspecific density? (2) If females manipulate
to offspring fitness can increase directly with the degree to which offspring size in response to density, is this response a general
competition is important (Hutchings 1991; Gliwicz and Guisande characteristic of H. formosa or a locally adaptive, plastic response
1992) or where densities are high (e.g., Berven and Chadra 1988; characteristic of populations that exhibit frequent and dramatic
Parichy and Kaplan 1992; Winn and Miller 1995; Marshall et al. changes in population density?
2006). We first tested the influence of differences in conspecific
Although increased size is advantageous for offspring, when density on offspring size and number using wild-caught females
there is a trade-off between offspring size and number, the opti- from the Wacissa River, Jefferson County, Florida, which had been
mal offspring size will be that which maximizes maternal fitness acclimated to laboratory conditions. This population exhibits reg-
rather than the size that maximizes fitness of individual offspring ular and extreme seasonal changes in population density, ranging
(Smith and Fretwell 1974; Parker and Begon 1986). In variable from high densities of 5000 individuals/m3 to low densities of
environments, optimal offspring size will vary (Brockelman 1975; < 20 individuals/m3 (Leips and Travis 1999; Richardson et al.
Parker and Begon 1986; Allen et al. 2008) and this may select for 2006). These large fluctuations in density should be a potent se-
phenotypic plasticity in offspring size via plasticity in maternal lective force favoring maternal adjustment of offspring size to
investment (McGinley et al. 1987; Fox et al. 1997), provided that maximize maternal fitness. We next compared the effect of den-
mothers can adjust the amount of energy devoted to each offspring sity on offspring size using females from the Wacissa River and
and that females have reliable cues predicting future environmen- a second, genetically distinct population, Trout Pond (Baer 1998;
tal conditions (reviewed in Ghalambor et al. 2007). Leips et al. 2000; Soucy and Travis 2003). Unlike the Wacissa
We explored the influence of conspecific density in the ma- River population, the Trout Pond population has a comparatively
ternal environment on offspring size using the matrotrophic, live- constant, low density rarely exceeding 30 individuals/m3 (Leips
bearing fish, Heterandria formosa. In this species, the dry mass and Travis 1999; Richardson et al. 2006).
of embryos increases nearly 50-fold from fertilization to birth
(Reznick and Miles 1989; Schrader and Travis 2005) and nearly
all of the energy required by the embryo is provided by maternal Materials and Methods
provisioning throughout development through a follicular pla- BIOLOGY AND NATURAL HISTORY
centa (Turner 1937; Fraser and Renton 1940; Grove and Wourms OF HETERANDRIA FORMOSA
1994). Females also exhibit superfetation, simultaneously carry- The least killifish (H. formosa), a member of the topminnow
ing multiple broods of offspring at different stages of develop- family Poeciliidae, is found in freshwater habitats throughout the
ment. The gestation period for this species is 27–35 days (Fraser southeastern United States. Long-term studies of H. formosa pop-
and Renton 1940; Scrimshaw 1944) and superfetation allows fe- ulations in north Florida have documented a number of dramatic
males to give birth continuously throughout a breeding season, differences among populations; most strikingly, variation in off-
with the interval between successive broods being as short as a spring size and number is associated with variation in average
few days (Cheong et al. 1984; Travis et al. 1987; Reznick et al. population density such that, in the highest density Wacissa River
1996). Extreme matrotrophy and superfetation, in combination, population, average offspring size is as much as 45% larger than
provide the opportunity for females to adjust their investment that of all other populations (Leips and Travis 1999). Differences
1342 EVOLUTION MAY 2009B R I E F C O M M U N I C AT I O N
among populations in offspring size at birth are driven by differ- Daphnia (3:1 ratio of flake food to Daphnia), 9.25 mg food per
ences in provisioning by the female after fertilization, particularly fish per day. We set up 12 tanks at each density for fish from
in the late stages of development (Schrader and Travis 2005). Trout Pond and six tanks at each density for fish from Wacissa
River. More Trout Pond replicates were set up because we had no
EXPERIMENT 1: DOES VARIATION IN MATERNAL prior data on this population, and we were simply trying to con-
DENSITY AFFECT OFFSPRING SIZE, COMPOSITION, firm the results obtained in Experiment 1 for the Wacissa River
AND NUMBER? population.
Wild-caught, adult H. formosa from the Wacissa River were hap- After six weeks at experimental treatment densities, offspring
hazardly assigned to either low (two males, two females) or high were collected every one or two days from all tanks for 44 days.
density (six males, six females) treatments in 21 L aquaria in a In this experiment, females remained in the high- and low-density
controlled-temperature (31◦ C) room on a 14:10 light:dark cycle treatments and all offspring were collected from each tank as they
at Florida State University. These densities are within the normal were produced because Trout Pond females had low survival when
range of densities experienced by fish in the Wacissa River. Fish isolated. Consequently, we were unable to determine whether ma-
were fed twice per day with 6.25 mg of ground TetraMin (Tetra ternal density influenced brood size in this experiment. Newborn
Werke, Melle Germany) fish flakes per individual and 0.25 mL of offspring (N = 797) were euthanized with MS-222 and frozen
frozen or newly hatched brine shrimp per individual every other individually in eppendorf tubes at −60◦ C. Samples were subse-
day. Fish were held under these conditions for six weeks, a period quently freeze-dried prior to weighing.
well within the usual adult life span of females (J. Travis, unpubl.
data). Given the approximately 28-day gestation period of this STATISTICAL ANALYSIS
species, all offspring that were developing in females at the time Experiment 1
of capture should have been born during this six-week period; we Because successive offspring produced by a given female are
assumed that characteristics of offspring born after this time were not independent, we analyzed treatment effects on the av-
mainly influenced by experimental density treatments. After six erage mass of all offspring produced by the female. None
weeks, we removed a single female from each tank (10 and 9 of the following were significantly correlated with offspring
females from high and low density treatments, respectively) and mass and consequently none were included as covariates in
isolated her in a 21-L aquarium, maintaining housing conditions the analyses: female mass, mean number of offspring per
and feeding regime as above. Aquaria contained vegetation and brood, and total number of offspring. The effect of maternal
cover to provide refuge for newly born offspring. Offspring pro- density on dry mass of offspring was analyzed in a mixed
duced by females were collected daily for the next three weeks. model analysis of variance (ANOVA) with the model, y =
We counted offspring as part of a single brood if they were born c + Trt + Tank(Trt)+ error, where y was ln[offspring dry mass],
over two consecutive days. Offspring were euthanized in MS-222 Trt was the fixed effect of maternal density (low vs. high) and
(Sigma-Aldrich, St. Louis, MO), frozen at −80◦ C, freeze-dried Tank(Trt) was the random effect of tank nested within treatment.
for 24 h, and weighed. The lean dry weight of each individual was The random effect of tank was necessary to account for different
measured by placing it in ether for 24 h, freeze-drying it again females from the same tank included in the analysis. Offspring
for 24 h, and reweighing it. Total lipid mass was the difference size was ln transformed to meet assumptions of ANOVA. Brood
between the offspring dry mass pre- and postlipid extraction. The size was analyzed using the same model, except y was the average
standard length of each female was measured at the end of the brood size per individual female in the three weeks following the
3-week period. density treatment. Because brood sizes are count data and ranged
from 1 to 8 offspring per brood, we transformed the count data
√ √
EXPERIMENT 2: IS THE PLASTIC RESPONSE to [ x + ( x+1)] (per Snedecor and Cochran 1989) where x
OF OFFSPRING SIZE TO MATERNAL DENSITY was the average number of offspring per brood produced by a
CONSERVED AMONG POPULATIONS? given female. Using the same model and data transformations,
For this experiment, we collected an independent set of adult we also evaluated the effect of maternal density on total number
H. formosa from the Wacissa River and from Trout Pond. These of offspring and total number of broods produced by females in
fish were shipped to the University of Toronto and their first the three weeks following the density treatment.
generation offspring were used in experiments. The effect of maternal density on the proportion of total
We used the same protocols as in experiment 1, except where mass that was lipids was analyzed in a mixed model ANOVA
noted. Housing aquaria were 19 L and kept in a walk-in envi- with the model: [log(total lipid mass) − log(total offspring dry
ronmental chamber at 26◦ C. Fish were fed twice daily with a mass)] = c + Trt + Tank(Trt) + error. We did not include off-
R
finely ground mixture of Tetra-Min fish flakes and freeze-dried spring dry mass as a covariate because lipid proportion scaled
EVOLUTION MAY 2009 1343B R I E F C O M M U N I C AT I O N
isometrically with offspring mass. Determination of isometry was Although the total number of offspring produced by females in the
based on the lack of any significant correlation between [log(lipid low-density treatment exceeded that for the high-density treatment
mass) − log(offspring mass)] and log(offspring mass) in our data by about 50%, this difference was not significant (F 1,12 = 2.48,
(r = − 0.16, P = 0.39) (Mosimann and James 1979). P = 0.14). However, we had low power to detect any but very
large differences in total offspring number (>70% chance of a
Experiment 2 Type II error for an effect of this size or smaller based on post-hoc
Mean dry mass of all offspring from a tank was used as the unit of power calculations outlined in Zar (1999, p. 193)).
replication in this experiment. As a result of some fish mortalities, If female H. formosa constantly adjust offspring size to
n = 4 and 5 for low- and high-density treatments, respectively, the potential competitive environment, it is possible that focal
of the Wacissa River population, and n = 11 and 12 for low- and females in this experiment began to respond to their three weeks
high-density treatments of the Trout Pond population. in isolation by reducing the size of their offspring. Given the
The effect of maternal density on the dry mass of offspring 27-day gestation period at these temperatures, this effect would
was analyzed in ANOVA with the model, y = c + Trt + Pop + be most apparent in offspring born late in the isolation period, and
Trt × Pop + error, where y was ln[average offspring dry mass], Trt could partially obscure the effects of our density manipulation.
was the fixed effect of maternal density, Pop was the fixed effect On average, offspring in later broods were smaller (least-squares
of the population from which fish originated, and Trt × Pop was means across all females producing three broods were 0.91 mg for
the interaction. The effect of maternal density on offspring num- the first brood, 0.95 mg for the second, and 0.74 mg for the third).
ber was analyzed using the same ANOVA model, with average A repeated measures ANOVA (using broods 1–3 for all females
offspring number per female in a tank substituted as the dependent that produced at least three broods; few females produced more
√
variable, y. Average offspring per female was transformed to [ x than three broods) confirmed that offspring size decreased over
√
+ ( x+1)] (per Snedecor and Cochran 1989) where x was the time (F 2,8 = 7.11, P = 0.02). The brood by treatment interaction
average number of offspring per female in a tank. We could not was not significant (F 2,8 = 0.49, P = 0.63), although power for
analyze the effects of density on brood size or number of broods this test was low.
in this experiment because females were reared together in a tank.
All statistical analyses were carried out using PROC MIXED EXPERIMENT 2
or PROC GLM in SAS 9.1 (SAS Institute Inc., Cary, NC) or As in Experiment 1, females in the high-density treatment pro-
JMP3.1.5. duced larger offspring (by 16%) than females at low density
(F 1,28 = 9.35, P = 0.005, Fig. 1). Wacissa River females pro-
duced offspring that were 10% larger than the offspring of Trout
Results Pond females at both densities. Although this difference was not
EXPERIMENT 1 significant (F 1,28 = 3.62, P = 0.07), the direction of the differ-
The average dry mass of offspring produced by females in the ence is the same as that observed in nature (Leips and Travis 1999;
high-density treatment was 26% larger than that of females in the Schrader and Travis 2005) and in common garden experiments
low-density treatment (F 1,12 = 5.92, P = 0.03, Table 1). This (Leips et al. 2000). There was no evidence of any interaction
difference was not attributable to differences in lipid content; the between population and density treatment (F = 0.0, P = 0.98).
proportion of dry mass attributable to lipids did not differ between Increased offspring size came at the cost of total offspring
treatments (F 1,11 = 0.64, P = 0.43). Females in the high-density number produced per female over the course of the experiment,
treatment had brood sizes 38% smaller than those in the low- as the average number of offspring per female was significantly
density treatment (F 1,12 = 7.31, P = 0.01). This result is consistent reduced at high density (mean ± SE, high density = 5.19 ± 0.54,
with the trade-off between offspring size and number identified low density = 10.81 ± 1.35; F 1,28 = 18.9, P < 0.001). This effect
in previous work (Leips and Travis 1999; Leips et al. 2000). reflects the trade-off seen in Experiment 1. Populations did not
Table 1. Effects of maternal density on offspring size, composition, and number for females from the Wacissa River in Experiment 1.
Data are mean values±1 SE.
∗ ∗
Density Offspring Percent Number of Total number Total number
size (mg) lipid offspring/brood of offspring of broods
Low 0.73±0.08 0.13±0.01 3.2±0.4 8.9±1.2 2.9±0.4
High 0.98±0.04 0.16±0.02 2.0±0.2 6.1±1.3 2.8±0.4
∗
Significant differences between treatments (PB R I E F C O M M U N I C AT I O N
could expect to experience. We think this is the case because our
field observations indicate that adults and juveniles use the same
habitat and, also, that densities change little over the 14 days
during which female investment in late stage embryos will most
influence size at birth. In addition, when adult population den-
sities are high, the densities of immature animals are also high
(Leips and Travis 1999). Production of more, but smaller, off-
spring in low-density environments is predicted to occur because,
at low density, small offspring should have fitness similar to larger
offspring and, because of the inherent trade-off between offspring
size and number, females would benefit from producing as many
offspring as possible (e.g., Fox et al. 1997). Therefore the plastic
response of H. formosa that we observed is consistent with a life
history that maximizes maternal fitness (Bradshaw 1965; Smith
and Fretwell 1974; Parker and Begon 1986).
Figure 1. Mean mass (± SE of untransformed data) for offspring Surprisingly, the patterns of plasticity in offspring size in re-
of females from Trout Pond and Wacissa River held at high and low
sponse to density were parallel, even though the two populations
density. Numbers beside symbols indicate sample size (tanks are
typically experience very different density regimes. Although we
replicates). Analysis of ln-transformed data revealed significant
main effects of density and population, but no interaction effect.
only tested two populations, our results suggest that this plastic
response may be an evolutionarily conserved trait in H. formosa.
differ in total offspring per female (mean ± SE, Wacissa R = This conserved response could be a nonadaptive, generic, phys-
8.09 ± 2.07, Trout Pond = 7.84 ± 0.91;F 1,28 = 0.02, P = 0.89), iological response to high density. However, this seems unlikely
and there was also no population by treatment effect (F 1,28 = because stress responses to high-density typically result in re-
1.22, P = 0.28). duced reproductive output (Weeks and Quattro 1991; Wingfield
and Sapolsky 2003 but see Moore and Jessop 2003) and in some
cases reduced offspring size (McCormick 1998). We found no
Discussion change in offspring number and an increase, rather than a de-
Female H. formosa adjusted the size of their offspring in re- crease, in offspring size. Alternatively, the same response may
sponse to the density of adult conspecifics, increasing the size of be adaptive in both populations. Densities in Trout Pond popu-
their offspring at higher densities. In fact, we found that females lations rarely, if ever, get as high as those in the Wacissa River
were so sensitive to population density that, in Experiment 1, off- (J. Travis, unpubl. data), but it may be that the critical “high”
spring size began to decline over the three weeks when the focal density needed to induce the female response is occasionally at-
females were in isolation after the density manipulation. Although tained in Trout Pond. By this interpretation, the highest densities
the adaptive significance of increased offspring size at higher in Wacissa River would be far above the threshold “high” density
densities was not tested directly in these experiments, previous needed to induce larger offspring sizes. This idea remains to be
work on H. formosa found that survivorship was positively cor- tested.
related with offspring size in a laboratory environment (Henrich A third explanation for the parallel reaction norms is that
1998) and a number of studies on other species have shown that only the reaction norm for the Wacissa River is adaptive and the
larger offspring perform better under competitive conditions (e.g., Trout Pond norm is a retained ancestral trait. Supporting this idea,
Hutchings 1991; Marshall et al. 2006; Allen et al. 2008; Bashey a model by Masel et al. (2007) shows that the evolutionary loss of
2008). Our results are counter to effects of resource limitation formerly adaptive plasticity may be slow. In addition, plasticity in
on offspring size in H. formosa (Reznick et al. 1996), indicat- resource allocation to offspring size may be maintained by genetic
ing that what we observed was not a simple response to resource correlations and/or selection, even when it is rarely advantageous
competition/limitation. An adaptive interpretation of our results is (Donohue et al. 2000; Bashey 2006). The relative importance of
that females produce larger offspring in higher densities because factors that maintain plastic responses to density are an important
the size of an offspring, relative to the size of its competitors, area of future research.
is an important determinant of offspring fitness in competitive
environments.
ACKNOWLEDGMENTS
For this plasticity to be adaptive, a female’s experience with We are grateful to N. (Brinlee) Martin for advice and assistance in all
density must predict the level of competition that her offspring phases of the experiments run at FSU. Thanks to M. Gunzburger for
EVOLUTION MAY 2009 1345B R I E F C O M M U N I C AT I O N
collecting and shipping Heterandria to Toronto and to T. Michalak for Ghalambor, C. K, J. K. Mckay, S. P. Carroll, and D. N. Reznick. 2007.
help in caring for fish and running the experiment at the University Adaptive versus non-adaptive phenotypic plasticity and the potential for
of Toronto. Thanks to M. McPeek and M. Pilkington for use of their contemporary adaptation in new environments. Funct. Ecol. 21:394–407.
microbalances and to C. Kerling for many hours of weighing. We thank Gliwicz, Z. M., and C. Guisande 1992. Family planning in Daphnia: resistance
J. Stamps and A. Winn for discussions and A. Winn for comments on a to starvation in offspring born to mothers grown at different food levels.
previous draft. Financial support was provided by NSERC (Canada) to Oecologia 91:463–467.
HR and JR, by NSF (USA) to JT (DEB 92-20849 and 99-03925), by CPB Gomez, J. M. 2004. Bigger is not always better: conflicting selective pressures
at UC Davis and PREA (Ontario) to HR, by L. Rowe, P. Abrams and T. on seed size in Quercus ilex. Evolution 58:71–80.
Day to JR, and the Department of Zoology at the University of Toronto Grove, B. D., and J. P. Wourms. 1994. The follicular placenta of the viviparous
to HR and JR by. fish Heterandria formosa. II. Ultrastructure and development of the
follicular epithelium. J. Morphol. 220:167–184.
Heath, D. D. and D. M. Blouw. 1998. Are maternal effects in fish adaptive or
merely physiological side effects? Pp. 178–201 in T. A. Mousseau and
LITERATURE CITED C. W. Fox, eds. Maternal Effects as Adaptations. Oxford Univ Press,
Allen, R. M., Y. M Buckley, and D. J. Marshall. 2008. Offspring size plasticity NY.
in response to intraspecific competition: an adaptive maternal effect Henrich, S., and J. Travis. 1988. Genetic variation in reproductive traits in a
across life-history stages. Am. Nat. 171:225–237. population of Heterandria formosa (Pisces, Poeciliidae). J. Evol. Biol.
Azevedo, R. B. R., V. French, and L. Partridge. 1977. Life-history conse- 1:275–280.
quences of egg size in Drosophila melanogaster. Am. Nat. 150:250– Holbrook, G. L., and C. Schal. 2004. Maternal investment affects offspring
282. phenotypic plasticity in a viviparous cockroach. Proc. Natl. Acad. Sci.
Baer, C. F. 1998. Species-wide population structure in a southeastern U.S. USA. 101:5595–5597.
freshwater fish, Heterandria formosa: gene flow and biogeography. Evo- Hutchings, J. A. 1991. Fitness consequences of variation in egg size and food
lution 52:183–193. abundance in brook trout Salvelinus fontinalis. Evolution 45:1162–1168.
Bashey, F. 2006. Cross-generational environmental effects and the evolution Jann, P., and P. I. Ward. 1999. Maternal effects and their consequences for
of offspring size in the Trinidadian guppy Poecilia reticulata. Evolution offspring fitness in the yellow dung fly. Funct. Ecol. 13:51–58.
60:348–361. Leips, J., and J. Travis. 1999. The comparative expression of life-history traits
———. 2008. Competition as a selective mechanism for larger offspring size and its relationship to the numerical dynamics of four populations of the
in guppies. Oikos 117:104–113. least killifish. J. Anim. Ecol. 68:595–616.
Benton, T. G., S. J. Plaistow, A. P. Beckerman, C. T. Lapsley, and S. Littlejohns. Leips, J., J. Travis, and F. H. Rodd. 2000. Genetic influences on experimental
2005. Changes in maternal investment in eggs can affect population dy- population dynamics of the least killifish. Ecol. Monogr. 70:289–309.
namics. Proc. R. Soc. Lond. B 272:1351–1356. Masel, J., O. D. King, and H. Maughan. 2007. The loss of adaptive plasticity
Bernardo, J. 1996. The particular maternal effect of propagule size, especially during long periods of environmental stasis. Am. Nat. 169:38–46.
egg size: patterns, models, quality of evidence and interpretations. Am. Magnhagen C., and E. Heibo. 2001. Gape size allometry in pike reflects
Zool. 36:216–236. variation between lakes in prey availability and relative body depth.
Berven, K. A., and B. G. Chadra. 1988. The relationship among egg size, Funct. Ecol. 15:754–762.
density and food level on larval development in the wood frog (Rana Marshall, D. J., C. N. Cook and R. B. Emlet. 2006. Offspring size effects medi-
sylvatica). Oecologia 75:67–72. ate competitive interactions in a colonial invertebrate. Ecology 87:214–
Both C., M. E. Visser, and N. Verboven. 1999. Density-dependent recruitment 225.
rates in great tits: the importance of being heavier. Proc. R. Soc. Lond. McCormick, M. I. 1998. Behaviorally induced maternal stress in a fish in-
B. 266:465–469. fluences progeny quality by a hormonal mechanism. Ecology 79:1873–
Bradshaw, A. D. 1965. Evolutionary significance of phenotypic plasticity in 1883.
plants. Adv. Genet. 13:115–155. McGinley, M. A., D. H. Temme, and M. A. Geber. 1987. Parental invest-
Bridges, T. S., and S. Heppell. 1996. Fitness consequences of maternal effects ment in offspring in variable environments: theoretical and empirical
in Strebliospio benedicti (Annelida: Polychaeta). Am. Zool. 36:132–146. considerations. Am. Nat. 130:370–398.
Brockelman, W. Y. 1975. Competition, the fitness of offspring, and optimal Meylan, S., and J. Clobert 2005. Is corticosterone-mediated phenotype devel-
clutch size. Am. Nat. 109:677–699. opment adaptive? Maternal corticosterone treatment enhances survival
Cheong, R. T., S. Henrich, J. A. Farr, and J. Travis. 1984. Variation in fecundity in male lizards. Horm. Behav. 48:44–52.
and its relationship to body size in a population of the least killifish, Moore, I. T., and T. S. Jessop. 2003. Stress, reproduction, and adrenocortical
Heterandria formosa (Pisces: Poeciliidae). Copeia 1984:720–726. modulation in amphibians and reptiles. Hormones Behav. 43:39–47.
Clutton-Brock, T. H. 1991. The evolution of parental care. Princeton Univ. Mousseau, T. A., and C. W. Fox. 1998. Maternal effects as adaptations. Oxford
Press, Princeton, NJ. Univ Press, NY.
Donohue, K., D. Messiqua, E. Hammond Pyle, M. S. Heschel, and J. Schmitt. Mosimann, J. E., and F. C. James. 1979. New statistical methods for allometry
2000. Evidence of adaptive divergence in plasticity: density- and site- with application to Florida red-winged blackbirds. Evolution 33:444–
dependent selection on shade avoidance responses in Impatiens capensis. 459.
Evolution 54:1956–1968. Naguib, M., A. Nemitz, and D. Gil. 2006. Maternal developmental stress
Fox, C. W., M. S. Thaker, and T. A. Mousseau. 1997. Egg size plasticity in a reduces reproductive success of female offspring in zebra finches. Proc.
seed beetle: an adaptive maternal effect. Am. Nat. 149:149–163. R. Soc. Lond. B 273:1901–1905.
Fraser, E. A., and R. M. Renton. 1940. Observations on the breeding and Parichy, D. M., and R. H. Kaplan. 1992. Maternal effects on offspring growth
development of the viviparous fish, Heterandria formosa. Q. J. Microsc. and development depend on environmental quality in the frog Bombina
Sci. 81:479–520. orientalis. Oecologia 91:579–586.
1346 EVOLUTION MAY 2009B R I E F C O M M U N I C AT I O N
Parker, G. A. and M. Begon. 1986. Optimal egg size and clutch size: ef- Snedecor, G. W., and W. G. Cochran. 1989. Statistical Methods, 8th edn. Iowa
fects of environment and maternal phenotype. Am. Nat. 128:573– State Univ Press, Ames.
592. Soucy, S., and J. Travis. 2003. Multiple paternity and population genetic struc-
Pen, L. J., I. C. Potter, and M. C. Calver. 1993. Comparisons of the food ture in natural populations of the poeciliid fish, Heterandria formosa. J.
niches of three native and two introduced fish species in an Australian Evol. Biol.. 16:1328–1336.
River. Environ. Biol. Fishes 36:167–182. Spitzer, B. 2004. Maternal effects in the soft scale insect Saissetia coffeae
Persson, L., J. Andersson, E. Wahlstrom, and P. Eklov. 1996. Size-specific (Hemiptera: Coccidae). Evolution 58:2452–2461.
interactions in lake systems: predator gape limitation and prey growth Stanton, M. L. 1984. Seed variation in wild radish: effect of seed size on
rate and mortality. Ecology 77:900–911. components of seedling and adult fitness. Ecology 65:1105–1112.
Reznick, D. N., and D. B. Miles. 1989. A review of life history patterns in Travis, J. 1981. Control of larval growth variation in a population of Pseudacris
Poeciliid fishes. Pp. 125–148 in G. K. Meffe and F. F. Snelson, eds. triseriata (Anura, Hylidae). Evolution 35:423–432.
Ecology and evolution of livebearing fishes (Poeciliidae), Prentice Hall, Travis J., J. A. Farr, S. Henrich, R. T. Cheong 1987. Testing theories of clutch
Englewood Cliffs, NJ. overlap with the reproductive ecology of Heterandria formosa. Ecology
Reznick, D., H. Callahan, and R. Llauredo. 1996. Maternal ef- 68:611–623.
fects on offspring quality in poeciliid fishes. Am. Zool. 36:147– Turner, C. L. 1937. Pseudoamnion, pseudochorion, and follicular pseudopla-
156. centa in poeciliid fishes. J. Morphol. 67:59–89.
Richardson, J. M. L., M. S. Gunzburger, and J. Travis. 2006. Variation in Weeks, S. C., and J. M. Quattro. 1991. Life-history plasticity under resource
predation pressure as a mechanism underlying differences in numeri- stress in a clonal fish (Poeciliidae: Poeciliopsis). J. Fish Biol. 39:485–
cal abundance between populations of the poeciliid fish Heterandria 494.
formosa. Oecologia 147:596–605. Wilbur, H. M., and J. P. Collins. 1973. Ecological aspects of amphibian meta-
SAS Institute Inc. 2005. Version 9.1, Cary, NC. morphosis: nonnormal distributions of competitive ability reflect selec-
Sakwinska, O. 2004. Persistent maternal identity effects on life history traits tion for facultative metamorphosis. Science 182:1305–1314.
in Daphnia. Oecologia 138:379–386. Wingfield, J. C., and R. M. Sapolsky. 2003. Reproduction and resistance to
Schrader M., and J. Travis. 2005. Population differences in pre- and post- stress: when and how. J. Neuroendocrinol. 15:711–724.
fertilization offspring provisioning in the Least Killifish, Heterandria Winn, A. A., and T. E. Miller. 1995. Effect of density on magnitude of
formosa. Copeia 2005:649–656. directional selection on seed mass and emergence time in Plantago
Scrimshaw, N. S. 1944. Embyronic growth in the vivaparous Poeciliid, wrightiana Dcne. (Plantaginaceae). Oecologia 103:365–370.
Heterandria formosa. Biol. Bull. 87:37–51. Zar, J. H. 1999. Biostatistical analysis. Prentice Hall, NJ.
Smith, C. C., and S. D. Fretwell. 1974. The optimal balance between size and
number of offspring. Am. Nat. 108:499–506. Associate Editor: J. Wolf
EVOLUTION MAY 2009 1347You can also read
