Abstract and Figures

All organisms face two fundamental trade-offs in the allocation of energetic resources: one between many small versus a few large offspring, and the second between present and future reproduction. Nowhere are these trade-offs more apparent than in the vast range of variation in the sizes of eggs and offspring exhibited among species of marine invertebrates. It has become increasingly clear that, in many taxa of marine organisms, there is also substantial intraspecific variation in the size of eggs and hatchings. This variation has largely been attributed to adaptive maternal effects. In theory, however, the inevitable conflicts of interest that arise in families of sexually reproducing organisms over the optimal distribution of parental resources among siblings could also account for much of this variation in egg and offspring size. Here, we explore the potential impacts of family conflict on offspring traits by comparing the life histories of two exemplar species of marine organisms, the polychaete Boccardia proboscidea and the gastropod Solenosteira macrospira, emphasizing how differences in modes of fertilization and parental care might influence the phenotype and, consequently, the fitness of offspring.
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SYMPOSIUM
Reproductive Biology, Family Conflict, and Size of Offspring in
Marine Invertebrates
Stephanie J. Kamel,* Fernanda X. Oyarzun
1,†,‡
and Richard K. Grosberg*
Department of Evolution and Ecology, University of California Davis, Davis, CA 95616, USA;
Department of Biology,
University of Washington, Seattle, WA 98195, USA;
Friday Harbor Laboratories, University of Washington,
Friday Harbor, WA 98250, USA
From the symposium ‘‘Evolutionary Paths Among Developmental Possibilities: A Symposium Marking the Contributions
and Influence of Richard Strathmann’’ presented at the annual meeting of the Society for Integrative and Comparative
Biology, January 3–7, 2010, at Seattle, Washington.
1
E-mail: foyarzun@u.washington.edu
Synopsis All organisms face two fundamental trade-offs in the allocation of energetic resources: one between many small
versus a few large offspring, and the second between present and future reproduction. Nowhere are these trade-offs more
apparent than in the vast range of variation in the sizes of eggs and offspring exhibited among species of marine
invertebrates. It has become increasingly clear that, in many taxa of marine organisms, there is also substantial intra-
specific variation in the size of eggs and hatchings. This variation has largely been attributed to adaptive maternal effects.
In theory, however, the inevitable conflicts of interest that arise in families of sexually reproducing organisms over the
optimal distribution of parental resources among siblings could also account for much of this variation in egg and
offspring size. Here, we explore the potential impacts of family conflict on offspring traits by comparing the life histories
of two exemplar species of marine organisms, the polychaete Boccardia proboscidea and the gastropod Solenosteira
macrospira, emphasizing how differences in modes of fertilization and parental care might influence the phenotype
and, consequently, the fitness of offspring.
Introduction
The trade-off between size and number of offspring
is the fundamental principle underlying virtually all
of contemporary life-history theory (Vance 1973a,
1973b; Smith and Fretwell 1974). Since a mother
can only allocate finite resources to her progeny,
how those resources are partitioned among offspring
both within and between clutches is a critical deter-
minant of her fitness. Whether selection favors the
production of a few large or many small offspring
depends on the optimal balance between size and
number of offspring, which in turn hinges on the
relationship between the size of offspring and their
fitness (Lack 1947; Smith and Fretwell 1974;
Christiansen and Fenchel 1979; Lloyd 1987).
Nowhere are these trade-offs more apparent than in
the vast range of variation in the sizes of eggs, offspring,
and clutches exhibited by marine invertebrates
(Thorson 1946; Strathmann 1985; Kohn and Perron
1994; McEdward 2000; Podolsky and Moran 2006).
Vance (1973a, 1973b) developed the theoret-
ical framework that still guides much of our cur-
rent thinking about parental investment and the
evolution of egg size and offspring size in marine
invertebrates (Strathmann 1985; Emlet and Hoegh-
Guldberg 1997; Levitan 2000; McEdward and Miner
2003). His model, based on a multi-way energetic
trade-off between egg size, duration of the larval
stage, and offspring mortality, predicts that disrup-
tive selection will favor either small, minimally pro-
visioned, planktonic feeding offspring, or large,
well-provisioned eggs and offspring. Subsequent
work shows that factors other than energetics (e.g.,
fertilization mode, benthic versus planktonic devel-
opment, post-settlement performance) affect the evo-
lution of egg size, post-zygotic parental provisioning,
Integrative and Comparative Biology, volume 50, number 4, pp. 619–629
doi:10.1093/icb/icq104
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and hatchling size (Christiansen and Fenchel 1979;
Perron and Carrier 1981; Grant 1983; Podolsky and
Strathmann 1996; McEdward 1997; Levitan 2000;
McEdward and Miner 2003; Marshall et al. 2006).
These refinements, however, still largely focus on
patterns of interspecific variation and generally
assume that stabilizing selection on size of eggs or
offspring should substantially limit intraspecific var-
iation for these traits (reviewed by Kohn and Perron
1994; Marshall and Keough 2008).
Nevertheless, over the past decade it has become
increasingly clear that, in many taxa of marine
organisms, there is substantial intraspecific variation
in size of eggs and hatchlings not only within and
among populations, but also within and among
broods of the same female (Gibson 1997; Ellingson
and Krug 2006; Gosselin and Rehak 2007; Marshall
and Keough 2007). Explanations for among-brood
variation in the size of offspring often focus on
the environmental factors influencing maternal
investment (Bernardo 1996; Moran and Emlet
2001), or on variation in the availability of resources
to planktonic larvae (Marshall and Keough 2007),
whereas the causes of within-brood variation are
virtually unexplored. The most common explana-
tions ascribe such variation either to non-adaptive
stochastic variation in provisioning (Rivest 1983) or
to a maternal bet-hedging strategy in unpredictably
varying environments (Geritz 1995; Marshall et al.
2008b).
The conflicts of interest that arise in families of
sexually reproducing organisms over the optimal dis-
tribution of parental resources among siblings
(Trivers 1974; Temme 1986; Mock and Parker
1997) represent an alternative, rarely considered,
but potentially widespread source of variation in
size of eggs, seeds, and offspring. These conflicts
emerge from the asymmetries in relatedness that
are inevitable consequences of sexual reproduction.
Given that a female is equally related to all of her
offspring, all else being equal, selection should favor
a uniform allocation strategy (Parker et al. 2002).
However, a given offspring is more closely related
to itself than to either its siblings or to her, and
would benefit from a greater share of parental re-
sources (Parker et al. 2002). Thus, while maternal
fitness might be optimized with an invariant size of
eggs, seeds, or offspring, competition over resources
between parent and offspring or among siblings can
oppose this source of stabilizing selection and pro-
mote variation in size within and among popula-
tions, individuals, and broods (Queller 1984a,
1984b; Shaanker et al. 1988; Mock and Forbes
1992; Mock and Parker 1997). The mating system,
in turn, and especially the degree of multiple pater-
nity within and among sibships, can further amplify
the scope and magnitude of these conflicts, as it re-
duces the average relatedness among offspring and
increases the incentive to harm siblings (Parker
et al. 2002).
In contrast to several studies on mammals (Haig
1993), terrestrial plants (reviewed by Shaanker and
Ganeshaiah 1997; Brandvain and Haig 2005) and
marine (Paczolt and Jones 2010) and freshwater
fishes (Schrader and Travis 2008), remarkably little
empirical attention has focused on distinguishing
whether intraspecific variation in size of eggs and
offspring among marine invertebrates represents
adaptive maternal effects (sensu Marshall et al.
2008b), or instead reflects family conflict (Kamel
et al. 2010; see Parker et al. 2002; Royle et al.
2004; and Rowe and Arnqvist 2002 for more general
reviews). This lack of attention may be due to the
perception that mates, parents and offspring, and
siblings have limited opportunities to interact in
the sea. In this article, we re-consider this view by
exploring the various ways that family conflict could
influence the expression and evolution of variation
in size of offspring in marine invertebrates, and
by evaluating the limited empirical evidence that
it does so.
Reproductive mode and arenas of conflict
Marine organisms exhibit an astonishingly diverse
array of reproductive modes, broadly divided into
differences in where fertilization occurs (external
versus internal) and where and how offspring devel-
op (planktotrophic, lecithotrophic, or direct).
Broadcast spawners shed both eggs and sperm into
the water; spermcasting species retain their eggs but
release sperm; hence like copulating species, are usu-
ally internally fertilized. Regardless of whether fertil-
ization occurs externally or internally, the larvae that
develop after fertilization may either be feeding
(planktotrophic) or non-feeding (lecithotrophic) as
they disperse in the plankton before settling and
metamorphosing into sessile or sedentary adults.
However, in contrast to externally fertilized species,
internally fertilized species can brood offspring until
they emerge as fully developed juveniles (direct de-
velopers). Brooding, in turn, can be internal, with
nutrient exchange occurring via placentas or analo-
gous structures, or external, in egg masses, capsules
or sacs (Thorson 1950).
These differences in reproductive mode funda-
mentally determine the arenas and opportunities
for conflict among family members. In broadcast
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spawners, for instance, parent–offspring and sibling
conflict ought to be rare, because offspring will have
little opportunity to influence parental allocation
decisions, and siblings disperse sufficiently widely
that they are unlikely to interact (for some excep-
tions see Keough 1984; Veliz et al. 2006). Family
conflict will thus emerge primarily as an intersexual
interaction, with males and females having different
optima with respect to gametic traits such as egg size,
sperm behavior, and the proteins that regulate ferti-
lizability (Levitan 2006; Bode and Marshall 2007;
Palumbi 2009). Conversely, in organisms that
brood or encapsulate their offspring there are more
extensive opportunities for family members to inter-
act. For instance, encapsulation engenders some of
the most extreme forms of parent–offspring conflict
and sibling rivalry (Thorson 1950), including con-
sumption of non-developing nurse eggs (oophagy),
and of viable siblings (adelphophagy) (Elgar and
Crespi 1992). Siblings not only compete for nutrients
provided by their parents, but also for resources that
are affected by the packaging per se, such as the
availability of oxygen (Lee and Strathmann 1998;
Strathmann and Hess 1999; Moran and Woods
2007; Brante et al. 2008).
The ubiquity of egg masses, capsules, and other
forms of encapsulation in marine invertebrates sug-
gests that competition among siblings will occur fre-
quently. A recent meta-analysis, spanning a broad
range of marine taxa, provided intriguing circum-
stantial evidence that encapsulation and internal
brooding enhance opportunities for parent–offspring
and sibling conflict to influence offspring size
(Marshall and Keough 2007). In direct-developing
species (many of which internally brood or encapsu-
late their offspring), the coefficient of variation (CV)
in offspring size is 14%, declining to 10% and
4% in lecithotrophic and planktotrophic developers,
respectively (Marshall and Keough 2007). In addi-
tion, internally fertilized lecithotrophs (still more of
which are brooders or encapsulators) exhibit a sig-
nificantly higher within-population CV in offspring
size than do externally fertilized lecithotrophs (none
of which provide arenas for siblings to interact di-
rectly). What remains to be seen is the extent to
which these correlations between variation in off-
spring size and developmental mode reflect various
forms of environmentally modulated phenotypic var-
iation (including adaptive maternal effects), or
whether parent–offspring conflict and sibling conflict
also play a central role in determining these correla-
tions. We now turn to two case studies that illustrate
how often-overlooked aspects of an organism’s
reproductive biology can decisively affect the charac-
ter and magnitude of family conflict.
Boccardia proboscidea
Ecology, reproduction, and development
Boccardia proboscidea (Hartman 1940) is a gonochoric
spionid polychaete commonly found on the west Coast
of North America, with a distribution extending
from British Columbia to Baja California (Hartman
1941; F. Oyarzun, unpublished data). Its range also
includes Japan, southern Australia, South Africa,
and Hawaii, all places where it appears to have been
introduced (Hartman 1941; Petch 1989; Sato-Okoshi
and Okoshi 1997; Sato-Okoshi 2000; Simon et al.
2009). Individuals are small (2 cm maximum
length) and typically inhabit the high and middle
intertidal zones, either in the upper 4 cm of sediments,
or in crevices and between barnacles. Tubes consist
of sand and mucus and can occur in aggregations
as dense as 20,000 m
2
. The worms live 12 months,
and reproduce between March and September in the
Northeast Pacific (F. Oyarzun, personal observations;
Gibson 1997). Females can store sperm for months,
and brood fertilized eggs in capsules that they attach
to the inside wall of their tubes (Hartman 1941,
F. Oyarzun, personal observations).
Some populations of B. proboscidea unambiguous-
ly exhibit poecilogonous development, in which con-
specific females produce offspring that differ with
respect to both trophic mode and, likely, dispersal
potential (Gibson 1997; Gibson et al. 1999). Females
have been categorized by the different proportions
of offspring they produce (Gibson 1997). Type I
females produce only planktotrophic offspring, dis-
persing larvae that feed on phytoplankton. Type III
females produce capsules that contain unfertilized,
non-developing nurse eggs (90% of total egg pro-
duction), and both planktotrophic and adelphopha-
gic progeny (Fig. 1A–C). Adelphophages consume
nurse eggs and can also cannibalize planktotroph sib-
lings developing in the same capsule (F. Oyarzun,
manuscript in review). Adelphophages spend little
time on the plankton or recruit directly to the sed-
iment after hatching. Type II females are extremely
rare, and produce capsules in which most eggs de-
velop as planktotrophs and the remaining 15% are
nurse eggs. Females of all types can reproduce mul-
tiple times within a season, producing 30 capsules
in a given event (F. Oyarzun, unpublished data).
Egg capsules of Types I and II females contain
40–50 larvae, and those of Type III females contain
nurse eggs and, on average, five developing larvae
(Gibson 1997).
Family conflict in marine invertebrates 621
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Sibling conflict
In B. proboscidea, the opportunities for sibling con-
flict depend on a female’s reproductive type. Types I
and II females produce dispersing larvae that feed in
the plankton, limiting opportunities for competition
among siblings for resources. Indeed, variance in off-
spring size, both within and among broods, is small
for these types (Gibson 1997).
Numerous factors indicate that sibling conflict
among offspring of Type III females should be
high. Experimental manipulations show that adel-
phophages, the cannibalistic larvae that feed on
nurse eggs and sibling planktotrophic larvae, grow
faster at higher concentrations of nurse eggs. Given
that the mean number of nurse eggs per embryo
in a capsule is lower than the number of nurse
eggs that results in the highest in vitro growth
rates, sibling competition should be frequent
(F. Oyarzun, manuscript in review). Indeed, the var-
iance in offspring sizes is high among adelphophages
(CV 20%; Gibson 1997) and, within a given cap-
sule, adelphophages can hatch out at different stages
of development (F. Oyarzun, unpublished data).
Adelphophages can also eat their planktotrophic
siblings, which cannot defend themselves or escape
from the capsule.
In B. proboscidea, mothers play an important role
in mediating sibling conflict. First, they control the
number of nurse eggs they allocate to capsules.
Second, larval release requires maternal assistance.
Females actively pull each capsule until it tears,
expelling the contents of each capsule from the
tube (F. Oyarzun, unpublished data), thus ending
the opportunity for ongoing cannibalism.
Parent–offspring conflict
Parent–offspring conflict should arise in this system
because the rate of cannibalism that maximizes
maternal fitness is generally lower than the one
that benefits individual cannibalistic offspring
(Parker et al. 2002). Sibling cannibalism provides a
net benefit to mothers if they gain in offspring
number due to enhanced survival of cannibals as
compared to the sibling victims that perish.
Nevertheless in most circumstances, sibling cannibal-
ism entails a high risk of direct fitness loss for the
mother (Hamilton 1964). Selection should thus favor
traits that control levels of sibling cannibalism
(Schausberger and Hoffman 2008).
Given that females control the timing of hatching
in B. proboscidea, the resulting phenotypes of the
offspring (i.e., the proportion of planktotrophs
Fig. 1 (A) Adelphophagic larva of B. proboscidea. (B) Type III capsule of B. proboscidea containing adelphophagic (a) and planktotrophic
(p) larvae and also several nurse eggs (ne). (C) Capsules of B. proboscidea still attached to parts of the mother’s tube. (D) Capsules
of B. wellingtonensis.
622 S. J. Kamel et al.
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versus adelphophages; the size of adelphopages) may
reflect the maternal optimum. At the least, mothers
can limit the scope for sibling competition. The
timing of hatching varies within and among females:
some capsules are opened even though many nurse
eggs still remain and offspring emerge at different
sizes and at different developmental stages
(F. Oyarzun, unpublished data). Early opening of
capsules could provide both nutritional resources
for the female (in the form of uneaten nurse eggs
that she can ingest), as well as planktonically dispers-
ing larvae, features that might be a response to lo-
cally unfavorable conditions. In any case, although
there appears to be little opportunity for offspring
to influence when they hatch they still could con-
sume more of their siblings than would be the ma-
ternal optimum.
Maternal control of hatching is not ubiquitous
in members of this genus, however. For example,
females of the Southern-hemisphere species
Boccardia wellingtonensis exhibit Type III reproduc-
tion, but mothers do not actively open capsules
(F. Oyarzun, personal observations). Instead of dis-
crete capsules, females produce strings of capsules
linked by thin walls which, over time, can break
down, permitting the offspring to escape (Fig. 1D;
F. Oyarzun, personal observations). These connec-
tions also allow adelphophages to move to adjacent
capsules and ingest other nurse eggs and plankto-
trophs. As a result, females may have less direct
control over the size, number and dispersal of their
offspring, although they might still be able to exert
control over the types and sizes of offspring by
modifying the distribution of nurse eggs and plank-
totrophs among individual capsules.
The contrasting opportunities for maternal control
over sibling and parent–offspring conflict in
B. proboscidea versus B. wellingtonensis, combined
with extensive variation in the packaging of offspring
in the Boccardia–Polydora complex (e.g., one large
egg sac, interconnected capsules, separate capsules)
(Blake 1969) raise the questions of whether this
variation leads to predictable differences in levels of
sibling and parent–offspring conflict, and how these
reproductive traits evolve in a phylogenetic context.
Is there a repeated evolutionary trend, both within
and among clades, in the mode of encapsulation and
resource control, or does the current distribution of
traits reflect the present status of an ongoing,
dynamic conflict between parents and offspring?
The answers to such questions depend upon vastly
improving our understanding not only of the phylo-
genetic relationships in taxa like Boccardia, but also
on the phylogenetic distribution of the behaviors and
life-history traits of parents and offspring.
Solenosteira macrospira
Ecology, reproduction, and development
Solenosteira macrospira (Berry 1957) is a gonochoric
intertidal buccinid whelk native to the northern Gulf
of California. Adult S. macrospira range from 35 to
45 mm in spire height (Brusca 1980), and live near
rocks in sandy or muddy substrates in the middle to
low intertidal zones (Gemmell et al. 1987). Buccinids
are generally scavengers or saprophytes and can often
be seen feeding on dead fish and invertebrates
(Gemmell et al. 1987). Individuals of S. macrospira
live for several years and reproduce between
February and May in the northern Gulf of California.
Solenosteira macrospira females package large
broods (more than 200 eggs) in durable chitinous
capsules and then attach these capsules exclusively
to the shells of male conspecifics during the course
of mating (Fig. 2; Gemmell et al. 1987). Oviposition
exclusively on males appears to be limited to some
insects and amphibians in which males exhibit be-
haviors that bolster their confidence in paternity
(Smith 1979a, 1979b). Based on sampling at three
sites separated by up to 200 km of open water,
S. macrospira appears to be one of the few species
of gastropod in which females oviposit exclusively on
males, despite sex ratios being nearly equal. Males
also do not obviously guard females before, during,
or after copulation (R.K. Grosberg and S.J. Kamel,
unpublished data).
Females typically attach 4–31 (x¼18.3; SD 13.2)
capsules per clutch. Laboratory studies show that
inter-clutch intervals range from 2 to 14 days,
and that well-fed females can produce as many as
Fig. 2 Female (left) and male S. macrospira in the laboratory.
Egg capsules nearly completely cover the male, barely
visible on the right.
Family conflict in marine invertebrates 623
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10 clutches (x¼6.5 2.9 SE) over a 2–3-month
interval (R.K. Grosberg and S.J. Kamel, unpublished
data). Virtually all of the eggs begin development
synchronously; however, most are consumed by
their capsulemates and, on average, 3–5 hatchlings
emerge from the capsules and crawl off of the brooding
male about a month after oviposition (R.K. Grosberg
and S.J. Kamel, unpublished data). In contrast
to evidence that B. proboscidea females cannibalize
their offspring, neither female nor male Solenosteira
macrospira engage in comparable behavior.
Sibling conflict
While parental protection increases offspring access
to limiting resources and potentially reduces preda-
tion risk, offspring are nevertheless confined to a
small space in which direct competition for resources
can occur (Mock and Parker 1997; Strathmann and
Strathmann 2006). Sibling cannibalism, the most
extreme form of sibling conflict, is surprisingly
common in animals that produce such nurseries
(Elgar and Crespi 1992; Mock and Parker 1997).
Killing a conspecific can reduce the intensity of
competition for access to limited resources, whereas
cannibalism provides additional nutrition.
Reduction in size of the brood in S. macrospira is
severe, with only 2.5% of the eggs surviving until
hatching (R.K. Grosberg and S.J. Kamel, unpublished
data). The size of the brood begins to decline by Day
7, with the highest rates of cannibalism taking place
between Days 7 and 24. This occurs because some
embryos within the case develop more rapidly than
others, and consume many of the remaining eggs
and more slowly developing embryos before exiting
the case. Field and laboratory observations over the
course of three breeding seasons show that cannibal-
ism in S. macrospira occurs only within capsules,
and does not extend to juveniles in other capsules
(R.K. Grosberg and S.J. Kamel, unpublished data).
Rates of cannibalism and consequently growth
within a capsule also vary across a season, resulting
in substantial differences in the size and number of
emerging hatchlings (Fig. 3; R.K. Grosberg and
S.J. Kamel, unpublished data). We collected develop-
mental data from newly laid, field-collected egg cap-
sules deposited early and late in the breeding season
that we reared in the laboratory at 188C. We mea-
sured 15 embryos from four capsules of an individ-
ual female (n¼5 females) every three days using a
calibrated ocular micrometer at 25under a dissect-
ing microscope. In clutches laid earlier in the repro-
ductive season, embryos emerge sooner and at a
smaller size, and levels of intracapsular cannibalism
are considerably lower than in clutches laid later on.
The increase in rates of cannibalism could at least
partly reflect changes in maternal allocation of re-
sources to capsules. However, there are no obvious
seasonal differences in patterns of maternal alloca-
tion, either in terms of egg size or number of eggs
per capsule. Why then do late-season offspring
emerge at a larger size than do offspring earlier in
the season? Why are they more likely to cannibalize
capsulemates? An intriguing possibility is that in-
creases in cannibalism are driven by decreased relat-
edness of siblings within capsules, brought about by
higher levels of polyandry and patrilineal diversity
within a capsule later in the season. Explicit genetic
tests of the incidence of polyandry in gastropods are
rare (reviewed by Baur 1998); however, the few avail-
able data indicate that it may be common (Gaffney
and McGee 1992; Paterson et al. 2001). In the case of
S. macrospira, we assessed the incidence of polyandry
by genotyping offspring at six microsatellite loci
(n¼228 capsules and 1400 offspring), and inferred
Fig. 3 Seasonal variation in (top) developmental rate and
(bottom) cannibalism rate of S. macrospira based on newly laid,
field-collected egg capsules reared at 188C. Size estimates are
pooled means SE of 15 offspring from four capsules from each
of five field-collected females, sampled every third day.
624 S. J. Kamel et al.
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the number of paternal genotypes within a capsule
with the sibship reconstruction program COLONY
(Wang 2004). Preliminary genetic analyses of embry-
os within field-collected S. macrospira egg capsules
reveal more than four alleles at some microsatellite
loci (the maximum number expected if a single male
fathers the entire clutch), suggesting that multiple
males sired the siblings within a capsule. Indeed,
these analyses show that the mean number of patri-
lines per capsule is 2.9 (range 1–6) (Fig. 4; S.J. Kamel
and R.K. Grosberg, unpublished data).
Parent–offspring conflict
Intrabrood sibling cannibalism represents a form of
maternal investment subject to both parent–offspring
and sibling conflict (Mock and Parker 1997; Parker
et al. 2002). The magnitude of this conflict in part
depends on the number of embryos a female places
within a brood’s nursery, whether offspring consume
a fixed versus a variable number of siblings, and the
relatedness of those offspring. Ecological context may
also influence the fitness costs and benefits of canni-
balism, and hence its expression (Elgar and Crespi
1992). For example, several studies show that the
degree of cannibalistic behavior, and the extent to
which cannibals discriminate among kin, varies
with nutritional status, such that nutritionally
stressed progeny are more willing to consume close
relatives than when they are well fed (Pfennig et al.
1993).
Polyandry, through its effects on the relatedness
of broodmates, also magnifies the scope for parent–
offspring and sibling conflict over maternal alloca-
tion of resources as well as for rates of cannibalism
(Clutton-Brock 1991; Elgar and Crespi 1992; Mock
and Parker 1997; Summers and Earn 1999; Loeb
et al. 2000). A female is equally related to all of
her offspring; however, when females use sperm
from multiple males to fertilize a clutch, the average
relatedness of siblings will decline below 0.5. If fe-
males mix sperm from different males, then the
greater the level of polyandry, and the more likely
it is that sibling interactions within a nursery or cap-
sule will involve half-siblings, rather than full-siblings
(McCauley and Odonnell 1984; Laurila and Seppa
1998). All else being equal, polyandry should favor
the evolution and expression of sibling cannibalism,
because the average inclusive fitness costs of consum-
ing a capsulemate should decrease as the average
relatedness among capsulemates declines, regardless
of whether siblings can distinguish full- from
half-siblings.
In S. macrospira, our preliminary data indicate
that the seasonal increases in rate of cannibalism
and in size at hatching are correlated with an in-
crease in the number of patrilines represented
within egg capsules. This increase may represent off-
spring acquiring more resources than the parental
optimum later in the reproductive season, fueled
by the declining inclusive fitness costs of consuming
related capsulemates. Alternatively, the increasing
levels of cannibalism may be consistent with a chang-
ing parental optimum, reflecting the increased effi-
ciency that larger hatchlings might gain by attacking
their preferred prey: barnacle spat that recruit early
in the snail’s reproductive season and continue to
grow. Disentangling the relative winners and losers
in this conflict remains a major challenge in this and
other species subject to multiple conflicts of interest
and will minimally entail characterizing how lifetime
reproductive success in females varies as a function
of offspring size.
Discussion
Egg size and offspring size have pervasive develop-
mental, ecological, and evolutionary implications for
marine invertebrates. For example, egg size is often
correlated with duration of the planktonic phase, so
that species with small eggs and a planktonic larval
stage should disperse considerably farther than do
species with large eggs (Kohn and Perron 1994;
Collin 2004). Differences in dispersal abilities have
been shown to influence population connectivity
(Baskett et al. 2007), range size (reviewed by Lester
et al. 2007), the potential for local adaptation
(Sanford and Worth 2009; E. Sanford and
Fig. 4 Distribution of the number of patrilines within individual
capsules of S. macrospira (n¼228 capsules). For each capsule,
an average of 10 offspring was genotyped at six loci. Paternal
genotypes were inferred using the sibship reconstruction program
COLONY (Wang 2004).
Family conflict in marine invertebrates 625
by guest on October 8, 2010icb.oxfordjournals.orgDownloaded from
M.W. Kelly, submitted for publication), as well as
rates of speciation and extinction (Palumbi 1994).
Variation in egg size and offspring size both
within and among populations may be caused by a
variety of mechanisms. For instance, there is striking
geographic variation in reproductive mode among
populations of B. proboscidea (F. Oyarzun, unpub-
lished data). All three types live in California; how-
ever, only Type III females (producing a mixture
of planktotrophs and adelphophages) are abundant
in Canada, Washington, Oregon, and Japan (Sato-
Okoshi and Okoshi 1997; Sato-Okoshi 2000;
F. Oyarzun, unpublished data). Several reproductive
traits, such as the number of capsules deposited per
female, the ratio of offspring types, and the number
of nurse eggs per capsule, also vary geographically
(Gibson et al. 1999; F. Oyarzun, unpublished data).
Females in populations at higher latitudes spend
more time with their capsules, brood for longer
periods and produce more nurse eggs per capsule
(F. Oyarzun, unpublished data). This intra specific
pattern of latitudinal variation more-or-less corre-
sponds to the interspecific pattern found in some
(but by no means all) groups of marine invertebrates
in which species living at higher latitudes tend
to exhibit a higher incidence of direct development
and invest more in protective structures such as
capsules than do more temperate species (Thomson
1878; Thorson 1950; Pearse et al. 1991; Pearse 1994).
The sources and adaptive significance of this var-
iation in B. proboscidea and many other species
remain elusive. Most studies emphasize the roles of
physiological stress, maternal size and nutritional
state, and quality of habitats on the size of eggs
and offspring, presumably reflecting changing,
condition-dependent maternal optima (Marshall
et al. 2008a). However, as we emphasize here, con-
flict between family members, especially between sib-
lings and between parents and offspring over access
to nutrients and other resources, can also generate
variation in size of offspring. The jury is out as to
whether the widely observed variation in size of off-
spring within and among broods represents adaptive
adjustments on the part of parents, or is an outcome
of an evolutionary tug-of-war among family mem-
bers. Marine invertebrates, with their unmatched di-
versity of reproductive modes, provide incisive
opportunities to investigate these complementary
hypotheses.
Multiple mating, relatedness, and conflict
The role of mating system and family conflict as
arbiters of offspring size has largely been ignored in
marine organisms, in which most theoretical and
empirical works have emphasized free-spawning
species for which there is little opportunity for sib-
lings to interact either with each other, or with their
parents (e.g., abalones and sea urchins) (Levitan
1996; Swanson and Vacquier 1998). For many
marine invertebrates, however, there is growing
evidence that both polyandry and extended kin asso-
ciations exist (Kamel et al. 2010). Thus, the condi-
tions required for conflict to influence life-history
evolution should be widely met in marine
invertebrates.
In B. proboscidea, as in other spionids, males
provide females with spermatophores, which
can be stored for several months before use (Rice
1978, 1981; So
¨derstro
¨m 1920). Although genetic
data characterizing the mating system in
B. proboscidea are not yet available, given its
habit of living in very dense aggregations, sperm
limitation seems unlikely, and multiple mating is
probably common. Similarly, in S. macrospira,
laboratory-reared females can deposit more than
10 clutches over a 2-month interval. The potential
to lay multiple clutches, along with high population
densities (4200 individuals/m
2
), imply that females
mate with different males during each mating
event. Laboratory studies, in which individual
females were placed with five males, confirm this
prediction: females copulated with at least two, and
sometimes all five, males over 5 days of observation
(R.K. Grosberg and S.J. Kamel, unpublished data).
Polyandry in these systems would have further
implications whereby the observed cannibalistic be-
haviors would be a vehicle for playing out genetic
conflicts of interest. In polyandrous species, kin se-
lection should favor cannibalistic individuals that can
assess the degree of sibling relatedness resulting in an
inverse correlation between the likelihood of canni-
balism and the relationships between cannibal and
victim (Pfennig 1997; Bilde and Lubin 2001). Thus,
both B. proboscidea and S. macrospira provide ideal
systems for studying the existence and mechanisms
of kin recognition and its role in mediating family
conflict.
Conclusions
In both terrestrial and marine systems, the expres-
sion and evolution of offspring size is subject to
manifold conflicts, whose importance depends upon
the venue for fertilization, developmental mode, and
mating system. The degree of conflict also hinges on
the ability of offspring to counteract parental strate-
gies, as well as the discrepancy between the parental
626 S. J. Kamel et al.
by guest on October 8, 2010icb.oxfordjournals.orgDownloaded from
optimum, and that of its offspring. Here, we have
highlighted the biology of two species for which con-
flict might play an important, and novel, role in
generating variation in offspring size. It remains to
be seen whether such conflicts play a comparable
role in other marine invertebrates, but the conditions
essential for family conflict to influence the evolution
and expression of life-history traits are far more per-
vasive than is presently assumed. To the extent that
this is true, the current theoretical framework for
interpreting both interspecific and intraspecific vari-
ation in marine invertebrate life histories should
be expanded to recognize that neither father nor
mother always knows best: sometimes the kids get
their way.
Acknowledgments
Thanks to Richard Strathmann for extensive discus-
sion of ideas and to two anonymous reviewers for
many useful comments.
Funding
National Science Foundation (grants OCE 0217304
and OCE 0623102 to R.R.S.); National Science
Foundation (grant OCE 0909078 to R.K.G.);
Mellon Foundation (to R.K.G.); Friday Harbor
Laboratories of the University of Washington.
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... This association is known as q3 the maternal size-offspring size (MSOS) correlation (reviewed by Rollinson and Rowe, 2015). Modern theories invoke sibling interactions, metabolic costs, provisioning efficiency, and survival cost to reproduction, among other factors, as adaptive explanations of this pattern (e.g., Parker and Begon, 1986;Sakai and Harada, 2001;Kamel et al., 2010;Jørgensen et al., 2011;Kindsvater et al., 2011). However, owing to the ubiquity of the MSOS correlation, a more general mechanism is expected to explain its occurrence, such as overhead costs (i.e., the energetic costs that are associated with the initiation of reproduction) and/or condition-dependent offspring provisioning coupled with metabolic factors (reviewed by Filin, 2015;Pettersen et al., 2015;Rollinson and Rowe, 2015). ...
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https://deepblue.lib.umich.edu/bitstream/2027.42/137413/1/evo00383.pdf
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