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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Reproductive Biology, Family Conflict, and Size of Offspring in
Marine Invertebrates
Stephanie J. Kamel,* Fernanda X. Oyarzun
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.
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.
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
Advanced Access publication August 26, 2010
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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.
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
. 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.
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
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.
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
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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
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
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
¨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
), 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
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.
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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.
Thanks to Richard Strathmann for extensive discus-
sion of ideas and to two anonymous reviewers for
many useful comments.
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). ...
... Thus, the different trade-off between number and size of offspring between populations may be related to mothers' fitness and site-specific environmental conditions. Females can allocate only finite resources to their progeny, and a critical determinant of females' fitness is how those resources are partitioned between offspring (Kamel et al., 2010). Indeed, in many taxa, environmental factors, such as temperature, explained the variability in this trade-off (Pettersen et al., 2019). ...
In most animal taxa, large mothers (or those with high nutritional status) produce large offspring, leading to a maternal size-offspring size correlation, that is, a positive correlation between maternal size and offspring size. Here, we used the natural variation in maternal size between three natural populations of Buccinanops deformis (a marine snail with direct development, nurse egg feeding, and a single embryo per egg capsule) to study maternal investment and offspring size. The main objectives were to compare offspring size and maternal investment traits within and between populations and to evaluate the relationship between maternal size and offspring size. Although not supported in every population, our results show that maternal size was positively correlated with offspring size, thus representing an example of the maternal size-offspring size correlation in a species in which there is no competition for food between capsule mates because only one embryo develops per capsule. These findings also suggest that in B. deformis larger mothers produce more offspring and provide their offspring with more resources, and that this between-population variation in offspring size is related to differences in the number of nurse eggs allocated per egg capsule and in egg capsule size. The ubiquity of the maternal size-offspring size correlation in B. deformis needs to be tested further across populations, because factors other than maternal size could influence offspring size variation in this marine gastropod.
... Gastrotrochs occur in irregular pattern. Modified chaetae develop in chaetiger V in late larvae (Söderström 1920, as Polydora natrix;Hartman 1941;Carrasco 1976;Woodwick 1977;Blake and Kudenov 1981;Duchêne 1984Duchêne , 1989Guérin 1991;Gibson 1997;Blake and Arnofsky 1999;Gibson and Smith 2004;Blake 2006;Kamel et al. 2010;Oyarzun and Brante 2015;Blake 2017). ...
... However, Sato-Okoshi (2000) reported that Japanese populations only show lecithotrophic development, with no (or a very short) planktonic stage after hatching. The larval morphology of this species agrees with the description of that of B. proboscidea documented in Hartman (1941), Woodwick (1977), Blake and Kudenov (1981), Gibson (1997), Gibson and Smith (2004), Kamel et al. (2010), and Oyarzun and Brante (2015). The dorsal pigment pattern of these larvae resembles that of the larvae of B. tricuspa (Hartman, 1939) described by Carrasco (1976, as B. proboscidea;fide Blake and Kudenov 1978), B. natrix (Söderström, 1920) described by Söderström (1920, as Polydora natrix), and B. columbiana Berkeley, 1927 described by Blake and Arnofsky (1999) and Blake (2006) in having a single row of mid-dorsal melanophores. ...
Full-text available
Planktonic larvae of spionid polychaetes are among the most common and abundant group in coastal meroplankton worldwide. The present study reports the morphology of spionid larvae collected mainly from coastal waters of northeastern Japan that were identified by the comparison of adult and larval 18S and 16S rRNA gene sequences. The molecular analysis effectively discriminated the species. Adult sequences of 48 species from 14 genera ( Aonides Claparède, 1864; Boccardia Carazzi, 1893; Boccardiella Blake & Kudenov, 1978; Dipolydora Verrill, 1881; Laonice Malmgren, 1867; Malacoceros Quatrefages, 1843; Paraprionospio Caullery, 1914; Polydora Bosc, 1802; Prionospio Malmgren, 1867; Pseudopolydora Czerniavsky, 1881; Rhynchospio Hartman, 1936; Scolelepis Blainville, 1828; Spio Fabricius, 1785; Spiophanes Grube, 1860) and larval sequences of 41 species from 14 genera ( Aonides ; Boccardia ; Boccardiella ; Dipolydora ; Laonice ; Paraprionospio ; Poecilochaetus Claparède in Ehlers, 1875; Polydora ; Prionospio ; Pseudopolydora ; Rhynchospio ; Scolelepis ; Spio ; Spiophanes ) of spionid polychaetes were obtained; sequences of 27 of these species matched between adults and larvae. Morphology of the larvae was generally species‐specific, and larvae from the same genus mostly shared morphological features, with some exceptions. Color and number of eyes, overall body shape, and type and arrangement of pigmentation are the most obvious differences between genera or species. The morphological information on spionid larvae provided in this study contributes to species or genus level larval identification of this taxon in the studied area. Identification keys to genera and species of planktonic spionid larvae in northeastern Japan are provided. The preliminary results of the molecular phylogeny of the family Spionidae using 18S and 16S rRNA gene regions are also provided.
... Some species incubate externally fertilized eggs, whereas in viviparous species, fertilization is internal followed by retention of post-zygotic stages (Blackburn 1992;Gillespie and McClintock 2007;Kalinka 2015). In viviparous species, siblings may have limited space and nutrients, and competition may be intense (Kamel et al. 2010;Kamel and Williams 2017). The offspring may also compete with the parent to gain greater control over resources (Trivers 1974;Crespi and Semeniuk 2004;Kalinka 2015;Kamel and Williams 2017). ...
... Parvulastra vivipara and P. parvivipara have asynchronous gamete production and fertilization and incubate embryos year-round (Byrne 1996;Byrne et al. 2003), so the reproductive outputs determined here for these species are likely to be an underestimate. Thus, the level of parental care influences offspring number, size, weight, and fitness in viviparous sea stars, similar to other marine invertebrates (Kamel et al. 2010). ...
Full-text available
In marine invertebrates that care for their young, the number of offspring is often correlated with adult size. The number, size, and mass of progeny relative to parent size were investigated in three asterinid sea star species that incubate their young in the gonads. Cryptasterina hystera has intragonadal planktonic-type lecithotrophic larvae with development supported by large eggs (440-µm diameter) and the juveniles are similar in size (655-µm diameter; coefficient of variation, CV = 6.89%). By contrast, Parvulastra vivipara and P. parvivipara have small vestigial larvae and small eggs (135–150-µm diameter) with offspring development supported by sibling cannibalism (matrotrophy). The juveniles in the gonads vary in size (500–5000-µm diameter, CV = 63.87 and 53.27%, respectively). All three species show a positive relationship between parent size and the number and size of juveniles. The allometry of brooding hypothesis that the number of progeny that can be cared for is (paradoxically) constrained in large adults due to space limitation was tested. In all species, the number of progeny increased with adult size, indicating that there are no allometric constraints on offspring incubation. To compare parental investment across the two modes of provisioning, the juvenile weight of C. hystera was used as a pro rata progeny unit. The matrotrophs had a higher reproductive output than similarly sized C. hystera. Of the hypotheses proposed to explain the evolution of parental care in marine invertebrates, none are broadly applicable to the viviparous asterinids because of the marked differences in their reproductive strategies.
... The direct costs and benefits of inbreeding to individuals can be modified by kin selection and evolutionary conflict within families (Kamel et al. 2010a). For example, inclusive fitness gained through kin recognition can be substantial and has been linked to settlement patterns that promote spatial associations of relatives in bryozoans and ascidians (Keough 1984;Grosberg and Quinn 1986). ...
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Many benthic marine invertebrates resemble plants in being modular and either sessile or sedentary, and by relying on an external vector to disperse their gametes. These shared features, along with recent evidence of inbreeding in these taxa, suggest that theory and practice bearing on the evolutionary costs and benefits of inbreeding for plants could advance our understanding of the ecology and evolution of invertebrate animals. We describe how the theory for the evolution of inbreeding and outbreeding could apply to benthic invertebrates, identify and compare techniques used to quantify inbreeding in plants and animals, translate relevant botanical concepts and empirical patterns to their zoological equivalents, and articulate predictions for how inbreeding might be associated with major axes of variation in sessile and sedentary marine invertebrates. The theory of inbreeding and outbreeding provides critical insight into major patterns of life-history variation in plants and holds similar promise as a complementary perspective on the evolution of reproductive traits, lifespan, ecological strategies , and dispersal in marine invertebrates. Extending what we have learned from plants to marine invertebrates promises to broaden the general study of mating systems.
... AH 1. Among-individual variation has no effect on group performance P 1. Measures of group success will not change significantly with increasing repeatability of behavior AH 2. Among-individual variation within a group negatively impacts group performance due to the resulting increase in mismatches among individuals in their preferences and priorities P 1. Measures of group success will decrease with increasing repeatability of behavior AH 3. Within-individual variation, rather than among-individual variation improves group performance P 2. Groups with greater repeatability of behavior will experience delays in consensus, increased dissent, physical conflicts, fission events, and social parasites AH 4. Group success leads to an increase in among-individual variation in behavior, as opposed to the reverse relationship P 1. Measures of group success will increase with increasing total behavioral variation in the group, but decrease with increasing repeatability of behavior P 1. Measures of group success will not be correlated with the repeatability of behaviors assayed prior to group formation, but will be correlated positively with repeatability when the behaviors are measured after group formation P 2. Time-series analysis will reveal that changes in metrics of group success precede changes in repeatability of behavior (Mattila and Seeley 2007;Oldroyd and Fewell 2007). The result that genetic diversity improves group performance may not apply to non-eusocial animal groups, because cooperation and group success can be thwarted by reduced relatedness via within-group conflict (Kamel et al. 2010;Krupp et al. 2011). However, the parallel between research on among-individual behavioral variation and research on genetic diversity remains useful because the hypothesized mechanism by which genetic diversity leads to improved group performance-increased efficiency in task allocation-may be a shared mechanism that also explains why groups with greater among-individual behavioral variation can outperform homogeneous groups (Jandt et al. 2014;Jeanson and Weidenmüller 2014). ...
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Studies of eusocial insects have extensively investigated two components of task allocation: how individuals distribute themselves among different tasks in a colony and how the distribution of labor changes to meet fluctuating task demand. While discrete age- and morphologically-based task allocation systems explain much of the social order in these colonies, the basis for task allocation in non-eusocial organisms and within eusocial castes remains unknown. Building from recent advances in the study of among-individual variation in behavior (i.e., animal personalities), we explore a potential mechanism by which individuality in behaviors unrelated to tasks can guide the developmental trajectories that lead to task specialization. We refer to the task-based behavioral syndrome that results from the correlation between the antecedent behavioral tendencies and task participation as a task syndrome. In this review, we present a framework that integrates concepts from a long history of task allocation research in eusocial organisms with recent findings from animal personality research to elucidate how task syndromes and resulting task allocation might manifest in animal groups. By drawing upon an extensive and diverse literature to evaluate the hypothesized framework, this review identifies future areas for study at the intersection of social behavior and animal personality.
... This species is a polychaete from the west coast of North America, with a distribution extending from British Columbia to Baja California (Hartman, 1941;Radashevsky et al., 2019). Today its range also includes Japan (Sato-Okoshi, 2000), southern Australia (Blake and Kudenov, 1978;Hewitt et al., 2004;Lleonart, 2001;Petch, 1995), South Africa (Robinson et al., 2005;Simon et al., 2010), Hawaii (Bailey-Brock, 2000, New Zealand (Read, 2004) and Spain (Fernández et al., 2006), all places where it appears to have been introduced (Kamel et al., 2010). Since the austral spring of 2008, the species has been detected in intertidal sewage-impacted sites in Mar del Plata (Argentina). ...
Biological invasions produce an invader population boom but are often followed by an invader population bust. The decrease of the invader abundance ends with the coexistence of native species and the invader or with repeated boom and bust events. In the southwest Atlantic, the polychaete Boccardia proboscidea invaded the coasts influenced by sewage discharge. We studied the change in the intertidal benthic community during the boom-bust dynamic of the Bo. proboscidea invasion. During the boom, the invader polychaete was dominant forming monoculture reefs. Species richness, diversity, and evenness indices decrease in the boom phase. During the bust of the Bo.proboscidea invasion, the decrease of organic matter allowed Br. rodriguezii to coexist with Bo. proboscidea. Beta diversity comparing boom with the bust phase showed a greater nesting (nestedness component); reflecting a process of species loss. We found that both boom and bust phases of the polychaete Bo. proboscidea invasion were mediated by sewage.
... For species that care for their young internally, offspring interact with the parent and may compete with siblings for limited resources; these interactions may influence size variation at birth (Schrader & Travis 2009;Kamel et al. 2010B). Parent-offspring conflict and sibling competition are more intense in species that provide extra-embryonic nutrition, a mode of parental care called matrotrophy (Frick 1998;Schrader & Travis 2009;Mercier et al. 2016;Ostrovsky et al. 2015;Kamel & Williams 2017). ...
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Sibling competition and developmental asynchrony may greatly influence the arrangement and size of offspring of marine invertebrates that care for their young. In Parvulastra parvivipara, an asterinid sea star that incubates its young in the gonads, sibling cannibalism supports post-metamorphic development. Offspring size varies within (coefficient of variation, CV = 22.6 %) and among (CV = 17.7%) the gonads. Confocal microscopy was used to visualize early embryos and oocytes, and revealed the presence of several developmental stages within individual gonads. The eggs were a mean diameter of 84 μm. The observation of a gastrula at 86 µm smaller than the largest egg observed (134 µm) suggests that terminal egg size varies. The appearance of early embryos surrounded by somatic cells suggests that they may receive nutrients through histotrophy. Sibling competition intensifies once the digestive tract is functional in the tiny juveniles which then start to consume siblings. The arrangement of the offspring in the gonads was observed using micro-computed tomography. The juveniles were oriented with their oral surface facing each other, presumably as a defensive strategy to protect themselves from being eaten. Periodic release of offspring in single or several cohorts indicates continual reproduction. Released and retained juveniles varied in size. It is not known what initiates birth but it may be mediated by sibling competition. Larger adults had a greater allocation to female reproductive output than smaller adults.
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The temporal pattern of juvenile release by two species of viviparous asterinid sea stars that incubate their young in the gonads was documented. Parvulastra parvivipara released juveniles (400–3000 µm diameter) in 1–5 cohorts. Parents produced large juveniles (>1000-µm) irrespective of adult size. Released juveniles were larger than the retained juveniles. Most Cryptasterina hystera offspring were released in one large clutch of similarly sized juveniles (732-µm mean diameter). After this initial release, the presence of large juveniles (944-µm mean diameter) in the gonads of C. hystera indicates that they are supported by matrotrophy, potentially through sibling cannibalism. The degree of parental investment additional to the egg in both species was estimated by using a matrotrophy index (MI, the ratio of juvenile and egg dry mass). As the eggs of P. parvivipara and C. hystera could not be isolated, the eggs of their congeners (P. exigua and C. pentagona, respectively) were used as a proxy to estimate the MI, the first application of this index to a marine invertebrate. The MI ranged from 597 to 55082 in P. parvivipara and 1.7–6.2 in C. hystera for juveniles across the different size classes. Matrotrophy and size variation of offspring may be characteristics of echinoderms that incubate their young.
The Foveaux Strait oyster (Ostrea chilensis) fishery in southern New Zealand comprises many localised populations (oyster beds) that have survived disease mortality and 150 years of fishing. The reproductive biology of O. chilensis underlies the assumption that these populations are self-recruiting. A three-year study using passive, artificial collectors deployed in a gradient design around an isolated natal population investigated the hypothesis of self-recruitment. Spat settlement patterns measured the distributions of competent larvae as indicators of dispersal. This research also investigated the relationship between settler and brooder densities. Settler densities were not predicted by direction along or across the current, distance from the focal population, or by brooder densities. Settlement was widespread, and settlement patterns imply greater dispersal and larval mixing than previously reported. The swift currents and variable pelagic larval duration may enhance mixing and connectivity between populations. Demographically open recruitment should provide some resilience to disease mortality and fishing.
A small vermetid gastropod broods capsules containing nurse eggs and embryos that develop into small veligers. A few of these veligers continue development and growth while nurse eggs and developmentally arrested sibling veligers disappear. Survivors hatch as crawling pediveligers and juveniles. None of the veligers, if removed from capsules, swim in a directed way or withdraw into their shells, indicating that even the developing veligers are unsuited for extracapsular life until they can crawl. The shells of arrested veligers decalcify while their siblings grow. Few of the developmentally arrested veligers that were isolated from siblings and fed algal cells resumed detectable growth. Nurse eggs rather than cannibalism provide most of the food, but full growth of developing veligers depends on limited sharing; arrest of some siblings is a necessary adjunct of the nurse-egg feeding. Here, two developmental outcomes for larvae produced by developmental arrest of some (often termed poecilogony) serves instead as a means of brood reduction. Brood reduction is often attributed to family conflicts resulting from genetic differences. Another hypothesis is that a mother who cannot accurately sort numbers of nurse eggs and developing eggs into capsules could rely on brood reduction to adjust food for her offspring. At the extreme, an entirely random packaging would produce a binomial distribution of embryos in capsules, a very uneven distribution of food per embryo, and some capsules with no embryos. Males have yet to be found in this species, but even if reproduction is asexual, selection could still favor brood reduction.
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There are a variety of proposed evolutionary and ecological explanations for why some species have more extensive geographical ranges than others. One of the most common explanations is variation in species’ dispersal ability. However, the purported relationship between dispersal distance and range size has been subjected to few theoretical investigations, and empirical tests reach conflicting conclusions. We attempt to reconcile the equivocal results of previous studies by reviewing and synthesizing quantitative dispersal data, examining the relationship between average dispersal ability and range size for different spatial scales, regions and taxonomic groups. We use extensive data from marine taxa whose average dispersal varies by seven orders of magnitude. Our results suggest dispersal is not a general determinant of range size, but can play an important role in some circumstances. We also review the mechanistic theories proposed to explain a positive relationship between range size and dispersal and explore their underlying rationales and supporting or refuting evidence. Despite numerous studies assuming a priori that dispersal influences range size, this is the first comprehensive conceptual evaluation of these ideas. Overall, our results indicate that although dispersal can be an important process moderating species’ distributions, increased attention should be paid to other processes responsible for range size variation.
Many life-history and developmental studies of marine invertebrates assume that eggs of species with nonfeeding larvae are large because they provide materials for rapid development. Using the sea urchin Heliocidaris erythrogramma which has 400 μm eggs and nonfeeding larvae, we removed an acellular, lipid-rich component from the blastula equivalent to ca. 40% of the egg volume and ca. 50% of the organic mass. Experimentally manipulated, reduced-lipid larvae survived well, developed in the usual time (3.5 d), and high percentages of the original numbers metamorphosed into anatomically normal juveniles. Control juveniles were larger at metamorphosis, grew more, and survived longer than siblings that lacked this lipid-rich material. Moderate increases in egg size in species with nonfeeding larvae may enhance postlarval performance significantly and therefore may reflect selection on early juvenile traits. The contrasts of our results and comparable experiments with feeding larvae suggests that egg size may play fundamentally different roles in species with feeding and nonfeeding larvae. The accommodation of materials reserved for the juvenile stage should be considered among hypotheses on evolutionary modification of developmental patterns.
Explains the brood reduction in fruits as a consequence of sibling rivalry and parent-offspring conflict. A general model is proposed to account for variation in brood size and to extend the models developed for animals to the plants to explore the conditions under which reduction in brood size might occur. Pre- and post-fertilization mechanisms by which parent and offspring exert control over brood size are described. -from Authors