Exclusive male care despite extreme female promiscuity and
low paternity in a marine snail
Stephanie J. Kamel* and Richard
Center for Population Biology,
Department of Evolution and
Ecology, College of Biological
Sciences, University of California, 1
Shields Ave, Davis, CA, 95616, USA
Males exhibit striking variation in the degree to which they invest in offspring, from merely provisioning
females with sperm, to providing exclusive post-zygotic care. Paternity assurance is often invoked to
explain this variation: the greater a male’s confidence of paternity, the more he should be willing to provide
care. Here, we report a striking exception to expectations based on paternity assurance: despite high levels
of female promiscuity, males of a marine snail provide exclusive, and costly, care of offspring. Remarkably,
genetic paternity analyses reveal cuckoldry in all broods, with fewer than 25% of offspring being sired by
the caring male, although caring males sired proportionally more offspring in a given clutch than any other
fathers did individually. This system presents the most extreme example of the coexistence of high levels
of female promiscuity, low paternity, and costly male care, and emphasises the still unresolved roles of nat-
ural and sexual selection in the evolution of male parental care.
Conflict, gastropod, mating system, parental care, paternity, polyandry.
Ecology Letters (2012)
One of the cornerstones of the theory of parental care is that, all
else being equal, the greater a male’s confidence of paternity, the
more he should be willing to invest in post-zygotic care of offspring
(Clutton-Brock 1991). Consistent with this prediction, several exper-
imental studies have shown that males adjust care according to their
perceived paternity (Neff & Gross 2001; Neff 2003; Mehlis et al.
2010). Variation in patterns of paternal care across species also
reveals the expected positive relationship between average paternity
and paternal investment (Moller & Cuervo 2000; Arnold & Owens
2002). In principle, to the extent that male care entails the loss of
future mating opportunities, the benefits accrued by a caring male
from increased offspring fitness must outweigh the costs to his
residual reproductive value (Queller 1997; Alonzo 2010).
Despite being taxonomically widespread, exclusive male care is
the rarest form of post-zygotic parental investment (Clutton-Brock
1991), presumably because males in most species maximise their
reproductive success by deserting females and acquiring additional
matings. In previously described examples of exclusive male care
where paternity has been characterised, including fishes (Jones et al.
1999, 2001), sea spiders (Barreto & Avise 2008), isopods, amphi-
pods, polychaetes (Reish 1957) and giant water bugs (Smith 1979),
males exhibit a variety of pre- and post-mating behaviours, such as
mate guarding, that eliminate or severely reduce cuckoldry in their
broods. This ensures that males are maximising their immediate
genetic benefits of caring by privatising care-giving behaviours
towards their own offspring.
In other settings, the social system can introduce uncertainty in a
given male’s paternity, especially where males guard nesting sites
that successive females visit (Birks 1997; Emlen et al. 1998). In blue-
gill sunfish, for example, ‘sneaker’ males trespass on nest sites
during spawning and release viable sperm without providing paren-
tal care (Neff 2003). Nevertheless, in all of these cases, average
paternity of the caregiver consistently exceeds 70%, and males in
these taxa might pay relatively low mating costs, as territoriality
itself can lead to increased mating opportunities (Ah-King et al.
2005). Where females prefer males that demonstrate care-taking
abilities, either through nest building (Soler et al. 1998) or the pres-
ence of eggs in their nests (e.g. Marconato & Bisazza 1986; Knapp
& Sargent 1989), such preferences can lead to the evolution of male
care even in the absence of high paternity (Alonzo 2012).
Gastropod molluscs exhibit a variety of parental care behaviours,
from brooding offspring in modified pouches (Hull et al. 1999) to
the production of egg capsules attached to the benthos (Pechenik
1986); however, males typically provide no post-zygotic investment
in offspring. The marine snail Solenosteira macrospira presents a
remarkably different scenario, in which females apparently oviposit
exclusively on conspecific males and are incapable of ovipositing on
themselves (Berry 1957; Houston 1978; Fig. 1). Despite extensive
sampling at multiple sites throughout the mating season, we have
never observed females carrying egg capsules (Table S1; Fig. S1; see
also Houston 1978). By the end of the annual reproductive season,
the shells of virtually all males are completely covered by egg cap-
sules, which they carry for up to a month. Within the fluid-filled
capsules, trophic egg and embryo cannibalism represents a major
source of maternally derived nutrition for developing offspring.
Explicit genetic analyses of gastropod mating systems are rare,
although the limited available evidence suggests that multiple mating
is common, and that clutches contain multiple patrilines (Gaffney &
McGee 1992; Paterson et al. 2001; Panova et al. 2010; Brante et al.
2011). However, multiple paternity in species with male care repre-
sents cuckoldry, which care-giving males should be selected to pre-
vent (Coleman & Jones 2011). This raises the question of whether
male care in S. macrospira is accompanied by extensive cuckoldry or
whether paternity assurance mechanisms prevail.
In this study, we experimentally manipulated egg-capsule load in
Solenosteira macrospira to determine whether carrying egg capsules is
costly to males, and therefore constitutes parental investment. We
then used microsatellite markers to quantify parentage and brood
composition and to ask whether the mating system of S. macrospira
differs substantially from the polyandrous mating system character-
© 2012 Blackwell Publishing Ltd/CNRS
Ecology Letters, (2012)doi:10.1111/j.1461-0248.2012.01841.x
istic of other gastropods that lack male parental care. We also char-
acterised temporal variation in patterns of paternity by comparing
parentage across broods in different stages of development. Our
results show that exclusive and costly male parental care occurs
despite considerable female promiscuity and very limited paternity
within cared-for broods.
MATERIAL AND METHODS
Solenosteira macrospira is an omnivorous marine whelk in the family
Buccinidae (Houston 1978), native to sandy mudflats of the north-
ern Gulf of California. Females and males are polygamous, with a
reproductive season that extends from February to June. Females
are internally fertilised, and package their offspring in chitinous cap-
sules, each containing ? 250 eggs. Mating pairs of S. macrospira
remain side-by-side, often for several hours or more, with the
female repeatedly extending her foot and head to deposit egg cap-
sules onthe male’s shell.
(mean = 18.3 ± 13.2) capsules per clutch. Females produce multiple
clutches during the reproductive season, and males carry clutches
from several different females (mean = 3.2 females, range: 2–5),
which can be distinguished by differences in colour, morphology,
and developmental stage of the embryos. Male parental care in S.
macrospira is essential for offspring survival as it reduces thermal and
desiccation stress during low tides, keeps egg masses from becom-
ing progressively buried and anoxic (Houston 1978) and reduces
tumbling and abrasion of egg capsules (personal observations).
About 1 month after oviposition, 3–10 crawl-away hatchlings
emerge from each capsule. Given that males carry capsules at differ-
ent stages of development, the period of care likely extends over
several months. We have never observed males attempting to
remove capsules, nor have we seen freshly laid capsules superim-
posed over older ones. Once offspring emerge, however, capsules
deteriorate in the time between reproductive seasons.
Measuring costs of parental care
To estimate the costs of egg-carrying by S. macrospira, we collected 169
male and 200 female adults in April 2004 from a 500-m-long site
2 km north of San Felipe (Baja California, Mexico). We collected only
those males completely covered by egg capsules; none of the females
had any egg capsules. We used a non-toxic marine-grade cyanoacrylate
adhesive to attach uniquely numbered, colour-coded Floy®(Floy Tag
Inc., Seattle, WA, USA) shellfish tags to all individuals, then weighed
each snail on a digital balance, after blotting it with dry paper towels.
We then removed all egg capsules from the males, and re-weighed
each individual. The males and females were then randomly divided
into a control and experimental group. The controls were left unma-
nipulated; in the experimental males and females, we used the same
non-toxic glue to attach enough egg capsules on to each snail’s shell
so that they were completely covered. We then weighed each of the
experimentally treated individuals. Both control and experimental
snails were tethered in the field with a 2-m length of monofilament
fishing line (tested to hold 8 kg) knotted through a small hole drilled
near the aperture of the snails’ shell, and anchored to the substrate
with a U-shaped 40-cm-long stainless steel rod. After 14 days in the
field, we recovered 70% of the originally tethered snails and re-
weighed them, allowing us to calculate net change in mass over the
course of the experiment. Using initial body weight as a covariate, we
performed a two-factor ANOVA using sex and capsule presence as fixed
factors to assess the treatment effect on the change of body weight.
We assumed that any changes in snail mass over the course of the
field experiment reflected the effects of the experimental manipula-
tions of egg capsules themselves, and were not due to the effects of
glue per se. The total mass of adhesive used to attach the capsules to
each individual contributed less than 5% of the total weight of the
reattached capsules (i.e. on the order of several capsules). Moreover,
comparable adhesives have never been reported to affect snail perfor-
mance, especially in open field systems where any toxic effects would
be quickly diluted (E. Carrington and D. Padilla, pers. comm.). Finally,
we performed control experiments on another predatory whelk of
similar size (Nucella ostrina), where we compared growth rates of glue-
covered vs. uncovered snails (n = 20 snails per treatment). We found
no significant effect of the glue on the change in mass between the
Genetic analysis of paternity and brood composition
We collected 287 adult male and female S. macrospira from Bahia de las
Chollas, near Puerto Pen ˜asco (Sonora, Mexico), in May 2005 to esti-
mate baseline population allele frequencies, and 15 egg-carrying snails
(all males) in April 2005 for paternity analysis. All snails were trans-
ported in coolers and returned alive to UC Davis. We genotyped
approximately 90 offspring from each of the 15 males (n = 1326 total
offspring from 43 different clutches) at six microsatellite loci (Table
S2). We assumed that each visually distinguishable clutch on a male’s
shell was produced by a different female, and we sampled clutches
from two to four females per male (Table S3). We categorised each
clutch as being composed of either early-stage (pre-veliger) or late-
stage (veliger) embryos. We also genotyped all of the offspring from a
subset of six clutches to determine the full extent of female promiscu-
ity. Each clutch was taken from a different male’s shell and corre-
sponded to a unique female. In addition to genotyping, the
developing embryos, we were able to genotype hatchlings collected
Figure 1 Male (left) and female (right) Solenosteira macrospira. The male’s shell is
completely covered with egg capsules. Photograph courtesy of P.B. Marko.
© 2012 Blackwell Publishing Ltd/CNRS
2 S. J. Kamel and R. K. GrosbergLetter
from 5 of the 15 males. These hatchlings were found crawling around
the shell of the care-giving male.
We extracted genomic DNA from ethanol-preserved muscle tis-
sue following the cetyltrimethyl ammonium bromide (CTAB) proto-
col described in (Grosberg et al. 1996). All PCRs were performed in
15 lL volumes using a GenAmp®9600 thermalcycler (Applied Bio-
systems, Carlsbad, CA, USA). PCR mixes consisted of 1.5–30 ng of
template DNA, 1x PCR Buffer, 2.5 mM MgCl2, 0.2 mM dNTP
(Promega, Madison, WI, USA), 0.1 mg/mL bovine serum albumin
(BSA, NEB), 0.25 lm forward and reverse primers, 0.6 U of
AmpliTaq®DNA polymerase (Applied Biosystems). The cycling
protocol consisted of an initial denaturation step of 3 min at 94 °C,
followed by 35 cycles of 94 °C denaturation for 30 s, annealing at
49 °C for 30 s and extension at 72 °C for 30 s. PCR products were
run on an ABI Prism 3100 Capillary Electrophoresis Genetic
Analyzer and analysed using the GeneScan software (Applied Bio-
systems, Carlsbad, CA, USA). Fragment data were visualised and
scored using STRand Version 2.3.69 (Toonen & Hughes 2001).
With the complete data set of 15 males and 1326 offspring, we used
COLONY (Wang 2004) to reconstruct sibships, to infer maternal
genotypes for all 43 clutches and to infer the number of sires per
clutch. We ran the analyses five times varying the random seed gen-
erator and the error rate; results did not vary across replicates. In
addition, we ran the analyses assuming no a priori information about
the number of mothers on a given male’s shell, allowing the pro-
gramme to independently estimate the number of contributing
females. This was done to validate our assumption that visually dis-
tinguishable clutches corresponded to different females. We also ran
the above analyses on the subset of females (n = 6), for which all
the offspring were genotyped.
The next step of the analysis involved using the reconstructed
maternal genotype obtained from COLONY and the egg-carrying
male’s known genotype to estimate his share of the paternity. We used
the population allele frequencies and equation (9) in Neff et al. (2000).
We also estimated paternity using a more conservative model, which
only uses the egg-carrying male’s genotype [see the two-sex paternity
model in Neff et al. (2000)]. For the hatchlings, we estimated the car-
ing male’s paternity using the two-sex paternity model, because we
could not be sure that all individuals came from the same mother.
The exclusion probability (the power of a locus to genetically exclude
candidate individuals as parents) for all six microsatellite markers
combined was 0.9931. We used linear regression analyses to test for a
relationship between male body size and total paternity. We used a
single-factor ANOVA to test for differences in paternity across develop-
mental stages and Student’s t-test to test for differences in paternity
between the care-giving male and the next most successful male.
We determined the relatedness (r) among siblings within a capsule
using the program STORM (Frasier 2008). This method was chosen
out of the many available approaches for calculating relatedness
because it is unbiased, it is never undefined and it consistently per-
forms well in a variety of situations, and often outperforms all other
estimators (see Frasier (2008) and references therein). In the absence
of inbreeding, the expected value of r for (1) unrelated individuals, (2)
parent-offspring or full-sibs and (3) half-sibs is 0, 0.5 and 0.25, respec-
tively. We used linear regression analysis to test for a relationship
between within-clutch relatedness and the number of sires. Where
applicable, results are presented as means ± standard deviations.
Costs of parental care
The capsules of a fully covered male represent approximately 40%
of a male’s wet mass (mean weight before capsule removal:
11.29 ± 1.32 g;weight aftercapsule
n = 139). Controlling for initial body size, we found a significant
negative effect of capsule presence on the change in snail weight
(F = 12.36, P < 0.001), which corresponded to a loss of approxi-
mately 8% of body mass. We also found a significant effect of sex
on change in weight (F = 58.46, P < 0.001), with manipulated
males losing more weight than manipulated females (Fig. 2). There
was also a significant interaction between capsule presence and ini-
tial weight (F = 5.00, P < 0.03), because snails with capsules were
all heavier than snails without.
removal:7.02 ± 0.85 g,
Distribution of paternity
The results of the paternity analysis were striking: on average, males
sired only 24% of the offspring they were carrying. Paternity esti-
mates varied widely among clutches, but never exceeded 61%
(range: 1–61%, which was found in 1 of 43 clutches; Table S3).
There was no significant relationship between male body size and
his proportion of clutch paternity (R2= 0.09, P = 0.29). In fact, a
given male could be simultaneously caring for the offspring of over
20 different males (Fig. 3). Paternity of the care-giving males was
significantly higher than the paternity of the next most successful
males (t-test: t = 4.06, P < 0.05).
The whole-clutch analyses of paternity revealed that female S. mac-
rospira are highly promiscuous, mating with 13.2 ± 2.1 males in a
Figure 2 Mean ± SD of the change in body weight, with and without
experimentally attached egg capsules on males’ and females’ shell in the snail
Solenosteira macrospira. Hatched bars represent individuals without egg capsules on
their shells, and black bars represent individuals with experimentally attached egg
© 2012 Blackwell Publishing Ltd/CNRS
LetterPaternity and male parental care 3
single breeding season (Table 1). Because of the high degree of
multiple mating in S. macrospira, the number of males that sired off-
spring in a given egg capsule ranged between one and six
(mean = 2.9 ± 1.1), and this number was negatively correlated with
the relatedness of offspring within a capsule (R2= 0.23, P < 0.001).
Mean paternity for clutches with the early-stage veligers was 22%
(95% CI: 13–32%), 29% (95% CI: 19–43%) for late-stage embryos
and 44% (95% CI: 28–71%) for hatchlings. There was no signifi-
cant difference in paternity between clutches containing early- and
late-stage embryos, but paternity of the genotyped hatchlings was
significantly higher than paternity in the early-stage clutches (ANOVA:
F2,45= 4.79, P = 0.01; Tukey post hoc test: P < 0.05).
This study confirms previous assertions (Houston 1978) that males
alone provide post-zygotic parental care in Solenosteira macrospira. As
demonstrated by the significant decrease in male body mass over
the course of 2 weeks of caring for capsules, egg-carrying exacts
substantial energetic costs. However, females in this species have
some of the highest documented levels of polyandry in an internally
fertilised organism (Gaffney & McGee 1992; Paterson et al. 2001;
Panova et al. 2010; Brante et al. 2011), with the number of sires per
clutch ranging between 6 and 15. Consequently, more than 70% of
the developing embryos that males care for are not their genetic
offspring. Furthermore, male body size, which often correlates posi-
tively with copulation duration and sperm transfer in other species,
did not predict paternity in our study (Simmons & Parker 1992).
This coexistence of extensive female promiscuity and costly male
parental care thus challenges general theoretical predictions of the
expected relationships between mating system, parental care and
Patterns of male care when paternity is high
In species where males carry eggs on or in their bodies, paternity is
usually certain. One of the best known examples of this is male
pregnancy in sygnathid fishes, where males are consistently the
genetic fathers of their offspring (Jones et al. 1999). Male care has
also evolved independently in at least 16 invertebrate taxa (Nazareth
& Machado 2010; reviewed in Tallamy 2000, 2001). Notable among
these are the pycnogonid sea spiders, in which uniparental care by
males is widespread. In all species studied to date, the male grasps
the female, with her gonopores held close to her partner. The eggs
are fertilised either while the female still holds them or immediately
after they have been deposited onto a male’s ovigers. In genetic
analyses of mating system in pycnogonids, there were no detectable
instances of cuckoldry (Barreto & Avise 2008). In contrast, egg-
carrying in the golden egg-bug Phyllomorpha laciniata appears to be a
form of intraspecific parasitism. Females deposit eggs fertilised by
another male on the current male’s back prior to mating, which
seems to be the price he pays to acquire a copulation (Kaitala &
Figure 3 Paternity breakdown for individual male Solenosteira macrospira. Black bars represent the caring male’s own proportion of total paternity, grey bars represent the
proportion of paternity for the next most successful male and white bars represent the proportion of paternity for all other males that sired offspring on that shell. The
number of sires included in the final group is indicated.
Table 1 Number of sires per clutch and average paternity of the caring male
from six clutches with all offspring sampled
Proportion of offspring sired by
© 2012 Blackwell Publishing Ltd/CNRS
4 S. J. Kamel and R. K. Grosberg Letter
In other systems, however, males adopt a strategy that involves
guarding nests or territories (Coleman & Jones 2011). This strategy
is common in many cichlids and sticklebacks, as well as arthropods,
in which males build nests and tend developing broods (Clutton-
Brock 1991; Tallamy 2001). In these cases, the rate of multiple
paternity is often skewed, with most species having low rates of
cuckoldry. That is, nest-defending males are usually the true sires of
most of the offspring in their nests.
Patterns of male care when paternity is low
The above examples of paternal care assume that investment in cur-
rent offspring decreases an individual’s ability to invest in future
offspring (Westneat & Sherman 1993), and that paternal care has
evolved because the benefits accrued by a caring male from
increased offspring fitness outweigh the costs to his residual repro-
ductive value. While many empirical studies support such a trade-
off between parental and mating effort, there are several instances
where such a trade-off appears not to exist; that is, investments in
parental care and mating effort do not conflict (Stiver & Alonzo
2009). For example, females of some species prefer males whose
nests already contain eggs (Marconato & Bisazza 1986; Porter et al.
2002), as it apparently indicates a willingness and ability to care for
young (Kvarnemo 2006). This preference is often so strong that
nest-guarding males may practice nest takeovers or egg thievery and
care for offspring that are not their own (Tallamy 2000; Nazareth &
Machado 2010; Coleman & Jones 2011). Indeed, recent theory pre-
dicts that if females are able to bias mating towards caring males,
male care will evolve even when the probability of males caring for
their own offspring is low (Alonzo 2012). Despite the theoretical
plausibility of the coexistence of male care, low paternity and female
promiscuity, S. macrospira provides one of the few, and perhaps only,
Causes of female promiscuity
It remains unclear why female S. macrospira are so polyandrous. Pre-
vious studies have documented that lower relatedness among sib-
lings can increase embryo survival, presumably because genetic
(McLeod & Marshall 2009; Sagebakken et al. 2011). However, the
high levels of documented promiscuity could be due to convenience
polyandry, where females assume the costs of additional matings
instead of expending time and energy attempting to reject harassing
males (Panova et al. 2010). Given that the genotyped embryos in
our study were all in the pre-hatching stages of development, we
could not evaluate the effects of genetic diversity on embryonic
traits or survival. However, sibling cannibalism and brood reduction
are severe in S. macrospira, with sibling cannibalism increasing with
increasing numbers of patrilines present among embryos within a
capsule (Kamel et al. 2010a). Females may mate with many males to
maximise phenotypic and genetic variance among siblings, thereby
increasing the scope for cannibalistic selection among offspring
within capsules to yield the fittest survivors (Elgar & Crespi 1992).
The fact that most surviving hatchlings were sired by a single male
is consistent with a particular paternal genotype winning out over
others. However, we also found evidence of last male sperm prece-
dence, because caring males sired proportionally more offspring in a
given clutch than any other fathers did individually. This simple
numerical advantage could have also lead to the increased represen-
tation of the caring male’s genotype in the hatchlings.
Temporal increases in female promiscuity might also explain this
pattern of high paternity among hatchlings. Given that the
hatchlings represent the most advanced stage of development, the
capsules we sampled were laid early in the season when females had
potentially mated with fewer males. Paternity could then be higher
simply by virtue of decreased sperm competition. However, pater-
nity of the caring male was low among late-stage embryos as well;
the increase occurred after offspring became cannibalistic. For now,
we can only speculate as to why more of the caring male’s offspring
emerge as the survivors. It might be that fathers can skew hatching
success in favour of their own young or that females choose a
high-quality male to mate with last. Alternatively, this pattern could
be generated by an age effect: older sperm could result in poorer
offspring survival, so the offspring of the last male to mate would
have higher survival, by virtue of being fertilised by younger sperm
(Blount et al. 2001). What is clear is that understanding the causes
of such promiscuity will be an important direction for future work.
Parental care as a constraint
The relationship between paternity and parental care also reflects the
evolutionary history of a species. The simplest explanation here
might be that, unlike in many other organisms (Kaitala & Kaitala
2001; Neff & Gross 2001), males cannot avoid caring for offspring.
Throughout most of the reproductive season, virtually all males are
covered with capsules; there does not appear to be a subset of chea-
ter males that acquires copulations without providing the requisite
caring behaviour. Interestingly, with the exception of S. macrospira and
its congeners, all other cantharid gastropods attach their eggs to hard
substrates in the intertidal (Houston 1978). The habit of attaching
eggs to conspecifics may have evolved due to the limited availability
of rocky substrate in intertidal areas of the northern Gulf of Califor-
nia, or as a way for adults to mitigate risks of predation or thermal
stress on developing offspring in these warm, shallow, subtropical
and tropical habitats. Males would be the primary targets for oviposi-
tion, given their proximity during copulation, and because conspecific
females and heterospecifics would have no incentive to allow attach-
ment of egg capsules. An inability for males to perceive or improve
their paternity could underlie the persistence of this trait (Maynard
Smith 1977; Westneat & Sherman 1993). However, it should not be
forgotten that each caring male is likely to sire young in the subse-
quent mixed-paternity clutches a female produces, which should pre-
sumably improve the cost:benefit ratio of care. Indeed, it is possible
that having offspring on other males’ shells might be an effective
form of bet-hedging from the focal male’s perspective.
A clear view of the true winners and losers in this conflict over
which parent assumes the burden of parental care requires a com-
prehensive understanding of the nature of sexual conflict over off-
spring care, including knowledge of the variance in lifetime
reproductive success, an enormous challenge in many species,
including S. macrospira, where a male’s offspring may be distributed
widely in space and time. Despite decades of extensive research on
parental care, our work provides the most extreme example of the
coexistence of high levels of female promiscuity, low paternity and
© 2012 Blackwell Publishing Ltd/CNRS
LetterPaternity and male parental care 5
costly male care. The behaviours exhibited by S. macrospira serve as
a reminder that observed patterns of parental care reflect not only
parentage, but also the interdependent outcomes of ongoing
conflicts of interest within and between the sexes, and between par-
ents and offspring (Parker et al. 2002; Kamel et al. 2010b), along
with phenotypic and genetic constraints on the expression and evo-
lution of parental investment (Alonzo 2010, 2012).
We thank B.B. Cameron, M.L. Loeb, A.C.C. Wilson and N.D. Tsut-
sui for assistance. We thank P.B. Marko for drawing our attention
to this system and its initial development. R.K.G is funded by NSF
(ANB041673 and OCE 0909078) and S.J.K. by an NSERC Post-
RKG designed the experiment and collected data. SJK collected
and analysed data. SJK wrote the first draft of the manuscript, and
both authors contributed substantially to revisions.
Ah-King, M., Kvarnemo, C. & Tullberg, B.S. (2005). The influence of
territoriality and mating system on the evolution of male care: a phylogenetic
study on fish. J. Evol. Biol., 18, 371–382.
Alonzo, S.H. (2010). Social and coevolutionary feedbacks between mating and
parental investment. Tree, 25, 99–108.
Alonzo, S.H. (2012). Sexual selection favours male parental care, when females
can choose. Proc. R. Soc. Lond. B, 279, 1784–1790.
Arnold, K.E. & Owens, I.P.F. (2002). Extra-pair paternity and egg dumping in
birds: life history, parental care and the risk of retaliation. Proc. R. Soc. Lond. B,
Barreto, F.S. & Avise, J.C. (2008). Polygynandry and sexual size dimorphism in
the sea spider Ammothea hilgendorfi (Pycnogonida: Ammotheidae), a marine
arthropod with brood-carrying males. Mol. Ecol., 17, 4164–4175.
Berry, S.S. (1957). Notices of new eastern Pacific Mollusca I. Leafl. Malacol., 1, 75–82.
Birks, S.M. (1997). Paternity in the Australian brush-turkey, Alectura lathami,
a megapode bird with uniparental male care. Behav. Ecol., 8, 560–568.
Blount, J.D., Moller, A.P. & Houston, D.C. (2001). Antioxidants, showy males
and sperm quality. Ecol. Lett., 4, 393–396.
Brante, A., Fernandez, M. & Viard, F. (2011). Microsatellite evidence for sperm
storage and multiple paternity in the marine gastropod Crepidula coquimbensis.
J. Exp. Mar. Biol. Ecol., 396, 83–88.
Clutton-Brock, T.H. (1991). The Evolution of Parental Care. Princeton University
Coleman, S.W. & Jones, A.G. (2011). Patterns of multiple paternity and
maternity in fishes. Biol. J. Linnean Soc., 103, 735–760.
Elgar, M.A. & Crespi, B.J. (1992). Cannibalism. Ecology and Evolution Among Diverse
Taxa. Oxford Science Publications, Oxford.
Emlen, S.T., Wrege, P.H. & Webster, M.S. (1998). Cuckoldry as a cost of
polyandry in the sex-role-reversed wattled jacana, Jacana jacana. Proc. R. Soc.
Lond. B, 265, 2359–2364.
Frasier, T.R. (2008). STORM: software for testing hypotheses of relatedness and
mating patterns. Mol. Ecol. Res., 8, 1263–1266.
Gaffney, P.M. & McGee, B. (1992). Multiple paternity in Crepidula fornicata
(Linnaeus). Veliger, 35, 12–15.
Grosberg, R.K., Levitan, D.R. & Cameron, B.B. (1996). Evolutionary genetics of
allorecognition in the colonial hydroid Hydractinia symbiolongicarpus. Evolution,
Houston, R.S. (1978). Notes on the spawning and egg capsules of two
prosobranch gastropods: Nassarius tiarula (Kiener, 1841) and Solenosteira
macrospira (Berry, 1957). Veliger, 20, 367–368.
Hull, S.L., Grahame, J. & Mill, P.J. (1999). Reproduction in four populations of
brooding periwinkle (Littorina) at Ravenscar, North Yorkshire: adaptation to
the local environment? J. Mar. Biol. Assoc. UK, 79, 891–898.
Jones, A.G., Rosenqvist, G., Berglund, A. & Avise, J.C. (1999). The genetic
mating system of a sex-role-reversed pipefish (Syngnathus typhle): a molecular
inquiry. Behav. Ecol. Sociobiol., 46, 357–365.
Jones, A.G., Walker, D., Kvarnemo, C., Lindstrom, K. & Avise, J.C. (2001).
How cuckoldry can decrease the opportunity for sexual selection: Data and
theory from a genetic parentage analysis of the sand goby, Pomatoschistus
minutus. Proc. Natl. Acad. Sci. USA, 98, 9151–9156.
Kaitala, V. & Kaitala, A. (2001). Altruism, intraspecific parasitism and reciprocity:
egg carrying in the golden egg bug. Ann. Zool. Fenn., 38, 223–228.
Kamel, S.J., Oyarzun, F.X. & Grosberg, R.K. (2010a). Reproductive biology,
family conflict, and size of offspring in marine invertebrates. Inter. Comp. Biol.,
Kamel, S.J., Marshall, D.J. & Grosberg, R.K. (2010b). Family conflicts in the sea.
Tree, 25, 442–449.
Knapp, R.A. & Sargent, R.C. (1989). Egg mimicry as a mating strategy in the
fantail darter, Etheostoma flabellare - females prefer males with eggs. Behav. Ecol.
Sociobiol., 25, 321–326.
Kvarnemo, C. (2006). Evolution and maintenance of male care: is increased
paternity a neglected benefit of care? Behav. Ecol., 17, 144–148.
Marconato, A. & Bisazza, A. (1986). Males whose nests contain eggs are
preferred by female Cottus gobio L (Pisces, Cottidae). Anim. Behav., 34, 1580–
Maynard Smith, J. (1977). Parental investment: a prospective analysis. Anim.
Behav., 25, 1–9.
McLeod, L. & Marshall, D.J. (2009). Do genetic diversity effects drive the
benefits associated with multiple mating? A test in a marine invertebrate. PLoS
One, 4, e6347.
Mehlis, M., Bakker, T.C.M., Engqvist, L. & Frommen, J.G. (2010). To eat or not
to eat: egg-based assessment of paternity triggers fine-tuned decisions about
filial cannibalism. Proc. R. Soc. Lond. B, 277, 2627–2635.
Moller, A.P. & Cuervo, J.J. (2000). The evolution of paternity and paternal care
in birds. Behav. Ecol., 11, 472–485.
Nazareth, T.M. & Machado, G. (2010). Mating system and exclusive postzygotic
paternal care in a Neotropical harvestman (Arachnida: Opiliones). Anim.
Behav., 79, 547–554.
Neff, B.D. (2003). Decisions about parental care in response to perceived
paternity. Nature, 422, 716–719.
Neff, B.D. & Gross, M.R. (2001). Dynamic adjustment of parental care in
response to perceived paternity. Proc. R. Soc. Lond. B, 268, 1559–1565.
Neff, B.D., Repka, J. & Gross, M.R. (2000). Parentage analysis with incomplete
sampling of candidate parents and offspring. Mol. Ecol., 9, 515–528.
Panova, M., Bostrom, J., Hofving, T., Areskoug, T., Eriksson, A., Mehlig, B.
et al. (2010). Extreme female promiscuity in a non-social invertebrate species.
PLoS One, 5, e9640.
Parker, G.A., Royle, N.J. & Hartley, I.R. (2002). Intrafamilial conflict
and parental investment: a synthesis. Phil. Tran. R. Soc. Lond. B, 357, 295–
Paterson, I.G., Partridge, V. & Buckland-Nicks, J. (2001). Multiple paternity in
Littorina obtusata (Gastropoda, Littorinidae) revealed by microsatellite analyses.
Biol. Bull., 200, 261–267.
Pechenik, J.A. (1986). The encapsulation of eggs and embryos by molluscs: an
overview. Am. Malac. Bull., 4, 165–172.
Porter, B.A., Fiumera, A.C. & Avise, J.C. (2002). Egg mimicry and allopaternal
care: two mate-attracting tactics by which nesting striped darter (Etheostoma
virgatum) males enhance reproductive success. Behav. Ecol. Sociobiol., 51, 350–
Queller, D.C. (1997). Why do females care more than males? Proc. R. Soc. Lond.
B., 264, 1555–1557.
Reish, D.J. (1957). The life history of the polychaetous annelid Neanthes caudata
(delle Chiaje), including a summary of development in the family Nereidae.
Pac. Sci., 11, 216–228.
Sagebakken, G., Ahnesjo, I., Braga Goncalves, I. & Kvarnemo, C. (2011).
Multiply mated males show higher embryo survival in a paternally caring fish.
Behav. Ecol., 22, 625–629.
© 2012 Blackwell Publishing Ltd/CNRS
6 S. J. Kamel and R. K. GrosbergLetter
Simmons, L.W. & Parker, G.A. (1992). Individual variation in sperm competition Download full-text
success of yellow dung flies, Scatophaga stercoraria. Evolution, 46, 366–375.
Smith, R.L. (1979). Paternity assurance and altered roles in the mating-behavior
of a giant water bug, Abedus herberti (Heteroptera, Belostomatidae). Anim.
Behav., 27, 716–725.
Soler, J.J., Cuervo, J.J., Moller, A.P. & De Lope, F. (1998). Nest building is a
sexually selected behaviour in the barn swallow. Anim. Behav., 56, 1435–1442.
Stiver, K.A. & Alonzo, S.H. (2009). Parental and mating effort: is there
necessarily a trade-off? Ethology, 115, 1101–1126.
Tallamy, D.W. (2000). Sexual selection and the evolution of exclusive paternal
care in arthropods. Anim. Behav., 60, 559–567.
Tallamy, D.W. (2001). Evolution of exclusive paternal care in arthopods. Annu.
Rev. Entomol., 46, 139–165.
Toonen, R.J. & Hughes, S. (2001). Increased throughput for fragment analysis
on an ABI 377 automated sequencer using a 100-lane RapidLoad membrane
comb and STRand software. BioTechniques 31, 31, 1320–1324.
Wang, J.L. (2004). Sibship reconstruction from genetic data with typing errors.
Genetics, 166, 1963–1979.
Westneat, D.F. & Sherman, P.W. (1993). Parentage and the evolution of parental
behavior. Behav. Ecol., 4, 66–77.
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