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CURRENT ISSUES – PERSPECTIVES AND REVIEWS
Kin selection and the Evolution of Mutualisms between SpeciesAndrew G. Zink
Department of Biology, San Francisco State University, San Francisco, CA, USA
(Invited Review)
Correspondence
Andrew G. Zink, Department of Biology, San
Francisco State University, 1600 Holloway
Ave., San Francisco, CA 94132, USA.
E-mail: zink@sfsu.edu
Received: October 29, 2014
Initial acceptance: November 28, 2014
Final acceptance: February 28, 2015
(M. Hauber)
doi: 10.1111/eth.12383
Keywords: Coevolution, hamilton, kin
selection, mutualism
Abstract
Hamilton’s theory of kin selection has revolutionized and inspired fifty
years of additional theories and experiments on social evolution. Whereas
Hamilton’s broader intent was to explain the evolutionary stability of
cooperation, his focus on shared genetic history appears to have limited
the application of his theory to populations within a single species rather
than across interacting species. The evolutionary mechanisms for coopera-
tion between species require both spatial and temporal correlations
among interacting partners for the benefits to be not only predictable but
of sufficient duration to be reliably delivered. As a consequence when the
benefits returned by mutualistic partners are redirected to individuals
other than the original donor, cooperation usually becomes unstable and
parasitism may evolve. However, theoretically, such redirection of mutu-
alistic benefits may actually reinforce, rather than undermine, mutualisms
between species when the recipients of these redirected benefits are
genetically related to the original donor. Here, I review the few mathe-
matical models that have used Hamilton’s theory of kin selection to pre-
dict the evolution of mutualisms between species. I go on to examine the
applicability of these models to the most well-studied case of mutualism,
pollinating seed predators, where the role of kin selection may have been
previously overlooked. Future detailed studies of the direct, and indirect,
benefits of mutualism are likely to reveal additional possibilities for apply-
ing Hamilton’s theory of kin selection to mutualisms between species.
Introduction
Hamilton’s theory of kin selection (1963, 1964a, b)
has revolutionized and inspired the last fifty years of
additional theories and experiments on social evolu-
tion. Both elegant and general in form, Hamilton’s
rule predicts that a trait decreasing the direct fitness of
an actor may nevertheless spread in a population. The
loss of direct trait replication through the focal indi-
vidual may be outweighed by increases in the fitness
of recipients with a shared genetic history, and subse-
quently, a probability of having the same genetic copy
of the trait. In its original 1963 form, mathematically
expanded in 1964, Hamilton’s rule can be expressed
as (r b > c) where c is the fitness cost to the actor
(for expressing the trait) and b is the fitness benefit
across all recipients (for receiving benefits of trait
expressed), devalued by the average genetic related-
ness r between actor and recipient. If satisfied, Hamil-
ton’s rule predicts that a trait will spread in a
population even when it reduces the direct fitness of
individuals expressing the trait. These components of
Hamilton’s rule have been carefully quantified in
some species, confirming the predictions of his theory
(reviewed in Bourke 2014).
While Hamilton’s broader intent was to explain the
evolutionary stability of cooperative behavior among
individuals, his focus on kinship appeared to limit the
application of his theory to populations within a sin-
gle species rather than across interacting species. As a
consequence, the theory has mostly been applied to
areas such as intragenomic conflict, multicellularity,
Ethology 0 (2015) 1–8 © 2015 Blackwell Verlag GmbH 1
Ethology
ethologyinternational journal of behavioural biology
and animal societies (reviewed in Abbot et al. 2011).
Because individuals found in different species have an
r value of zero, explanations for altruism between
species has relied on other theories of cooperation
such as reciprocity (delayed return of altruistic bene-
fits; Trivers 1971), by product mutualism (incidental
altruism via selfish action; Bshary & Bronstein 2004),
or partner choice (choosing to interact with the most
altruistic individuals; Bull & Rice 1991) rather than
Hamilton’s rule (Sachs et al. 2004).
These evolutionary mechanisms for interspecies
altruism, such as partner choice and reciprocity,
require spatial and temporal correlations among inter-
acting partners for benefits to be both predictable and
of sufficient duration to be delivered reliably. As a
consequence when the benefits returned by mutualis-
tic partners are redirected to individuals other than
the original donor, cooperation is likely to become
unstable and parasitism rather than mutualism may
evolve (Bull and Rice 1991, Herre et al. 1999, Bron-
stein 2001a,b). However, such redirection of mutual-
istic benefits may reinforce, rather than undermine,
mutualisms between species when the recipients of
returned benefits are genetically related to the origi-
nal donor within their focal species (Frank 1994; Fos-
ter & Wenseleers 2006; Queller 2012, 2014). This may
be a diffuse return on benefits (spread across multiple
kin as well as the original donor) or it may be a more
complete redirection, with kin of the original donor
receiving all of the returned benefits through redi-
rected reciprocity (Fig. 1). This process, in theory,
makes kin selection complementary to other mecha-
nisms for the evolution of mutualism such as reci-
procity.
Hamilton himself did not recognize the applicabil-
ity of his theory of kin selection to the evolution of
mutualisms between species. For example, in his
1972 paper, he emphasizes the important connec-
tion between offspring care and mutualistic gut bac-
teria in termites but he dismisses the role of kin
selection because bacteria and termites lack a shared
genetic history. Instead, Hamilton suggests that
other mechanisms such as reciprocity and partner
choice are likely to drive altruism between species
(Trivers 1971; Hamilton 1972). In this same paper,
however, Hamilton (1972) concludes the rapid
evolution of symbiotic bacteria within a long-lived
host. He outlines the idea that genetic diversity of
symbionts via horizontal transmission will maintain
virulence (parasitism), while symbiont lineages that
are vertically transmitted should evolve to be more
mutualistic. Without directly stating the role of kin
selection, Hamilton considers the evolution of mutu-
alistic (versus parasitic) bacteria more likely when
lineages within hosts have high genetic relatedness.
Hamilton’s (1972) insight regarding microbial sym-
bionts is reflected in recent studies outlining how
microbes reinforce social interactions while simulta-
neously influencing the costs and benefits of sociality
(Archie & Theis 2011). Recent evidence suggests that
microbes can even be a mechanism for kin recogni-
tion in some mammals, such as in the scent marking
of territories in hyenas (Theis et al. 2012). Other
researchers have suggested that social (kin) transmis-
sion of important symbionts, that help process plant
material, have been essential in maintaining sociality
in herbivores ranging from termites to ungulates (Tro-
yer 1984; Lombardo 2008). In addition, because
microbes themselves can be highly social, genetic
similarity may affect communication and cooperation
among colony members (Griffin et al. 2004). Ulti-
mately, this social behavior of microbes may also
influence how resources are transferred to or obtained
from the tissues of the microbe’s host organism (Mitri
& Foster 2013). However hosts are not passive part-
ners in this interaction; their physiology may favor
beneficial strains of microbes over less beneficial
strains, as a form of partner choice (Schluter & Foster
2012).
Here, I review the handful of mathematical models
that use Hamilton’s theory of kin selection to predict
(+)
(+)
r
Fig. 1: Simplest form of kin selection as a mechanism maintaining
mutualism between species. Focal (white) altruist gives benefits to reci-
pient individual in partner species (black) which returns benefits not to
original donor but rather a third individual with some kinship (r) to origi-
nal donor. In this case, a low value of r can undermine the benefits of
mutualism for the original donor. Conversely, a low positive return to
kin (from receiver of other species) can undermine the positive effects
of kin selection (even with a high r value).
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Kin Selection and Interspecific Mutualism A. G. Zink
the evolution of mutualisms between species. I then
explore the applicability of these models to the most
well-studied case of mutualism: pollinating seed pre-
dators, a system where the role of kin selection may
have been previously overlooked.
Mathematical Models
Thirty years after Hamilton’s original paper, Frank
(1994) became the first to formalize the notion that
genetic correlations among kin within populations
could facilitate the evolution of mutualisms between
species. Frank’s (1994) model is based on genetic cor-
relations among quantitative traits found both within
and across species, using the Price equation (Price
1970; Frank 1995). His model reveals that genetic cor-
relations between mutualistic traits found in different
species can act to increase the probability that benefits
will be returned to close kin (when they are not
returned to the original donor per say). Conversely,
this process also reinforces sociality within a focal spe-
cies via kin selection (routed through a mutualistic
partner) as long as the partner species has a high like-
lihood of interacting with kin of the original donor
(Frank 1994). Frank’s major insight, therefore, is that
altruistic alleles found in different species can build up
spatial and temporal associations (linkage disequilib-
rium) across species boundaries through kin selection
as the primary evolutionary mechanism.
Frank (1994) begins his model by defining a quanti-
tative trait (i) for mutualism, rearranging Hamilton’s
(1963) rule (r b > c) by defining genetic relatedness (r)
as the overall regression of average group trait values
is on individual trait values i:
risiðp1 � p2Þ > c
Here Frank has defined the benefits (b) of a mutual-
ism trait as p1 * p2 where p1 represents the average
amount of mutualistic aid given by individuals in the
focal group to individuals of a second species. Corre-
spondingly, the variable p2 is defined as the average
amount of mutualistic aid returned from the second
species to the original focal species group. As a result,
the aggregate benefit returned to individuals in the
focal species can be defined as the product of these
two variables (p1 * p2), which must be balanced
against the direct cost (c) incurred by individuals
expressing the mutualistic trait (i) in the focal species
group. Expanding this process, Frank (1994) shows
that aid returning from the host (p2) can also depend
on genetic relatedness within that second species
group, resulting in kin selection for mutualistic traits
on both sides of the species divide. Frank (1997) also
has developed a more specialized model for the evolu-
tion of symbiosis, by considering hosts as an extended
phenotype (Dawkins 1982) of endosymbionts where
kinship among symbionts can influence the evolution
of mutualism toward hosts.
It was over a decade before a subsequent model of
interspecies mutualism was published that included
within-species kinship as an important factor (Foster
& Wenseleers 2006). This model focused on three
key factors in mutualism evolution: within-species
relatedness, between-species fidelity, and the benefit-
to-cost ratio of mutualistic traits. The model also
incorporated three mechanisms in mutualism evolu-
tion: cooperator association (genetic correlations aris-
ing over longer evolutionary time periods), partner
fidelity feedback (spatial correlations within a genera-
tion), and partner choice (choice of potential mutual-
ists in real time). The authors conclude that long-term
genetic correlations are likely overpowered by partner
fidelity feedback and partner choice within a single
generation, but concede that kin selection would
allow for genetic correlations to arise across species
boundaries after many generations (Foster & Wense-
leers 2006). Importantly, while partner choice and
fidelity feedback may reinforce mutualism via kin
selection in the short-term, these same two mecha-
nisms may also counteract kin-selected benefits of
mutualism when individuals choose partners within
their species that are non-kin.
Queller (2011,2014) has also published two more
recent models that consider how kin selection may
reinforce mutualisms between species. The first of
these two models (Queller 2012) extends Hamilton’s
rule to green beard genes as well as mutualisms
between individuals in different species (which he
calls ‘kith’). Like Foster & Wenseleers (2006), Queller
also highlights partner fidelity feedback and partner
choice as important mechanisms for maintaining
cooperation, recognizing that these mechanisms can
facilitate correlation between altruistic traits across
species boundaries. While traditional kin selection
does not necessarily require a recipient of altruism to
express the altruistic trait, but rather have a copy of
that trait in its genome, ‘kith’ selection does require
that benefits be returned from the second species to
others in the focal population (i.e., kin of the original
donor; Queller 2012). This result is similar to Frank’s
(1994) model, where p2 (return of benefits by mutual-
ist species) must be greater than zero for mutualism to
evolve via kin selection. As Queller points out, this
process becomes much more complicated when mul-
tiple species are involved, such as a microbiome or a
community of pollinating insects (Queller 2012).
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A. G. Zink Kin Selection and Interspecific Mutualism
In a more recent model, Queller (2014) considers
joint phenotypes (e.g., mother and offspring, mating
pairs) in the context of extended phenotypes (Daw-
kins 1982; Bailey 2012) using Fisher’s fundamental
theorem of natural selection as generalized by Price
(1970). Similar to Frank (1994), one outcome of this
model is linkage disequilibrium across species bound-
aries, with correlations building over time between
mutualistic traits found in each species. Queller views
the outcome of this process as a joint polygenic trait
where alleles contributing to the joint (extended)
phenotype just happen to be found in different spe-
cies. Additional examples of these extended pheno-
types can be found in a recent review paper by Bailey
(2012). While these traits found across species could
be additive in nature, they could also involve some-
thing akin to ‘intergenomic epistasis’ as originally out-
lined by Wade (2007) in the context of coordinated
dispersal traits by mutualist species. Queller makes a
similar point by using Wright’s adaptive landscape to
consider two traits with different fitness peaks across
each of two mutualistic species. He envisions these
traits being tethered to each other through epistasis in
their shared joint (extended) phenotype. Therefore,
these mutualistic traits may never reach an optimum
in their own (within species) adaptive landscape, due
to their shared phenotype with a partner species that
itself has mutualistic traits constrained within its own
adaptive landscape (Wade 2007; Queller 2014). I
would add that the fitness landscape itself is likely to
change (within a focal species) based on the fre-
quency of traits present in the partner species, leading
to a landscape that is animated over a fourth dimen-
sion (e.g., time) as allele frequencies change.
Two final models, recently published, are also
worth a mention. Fitzpatrick (2014) approaches the
situation of covariance between traits in a host and its
symbiont as analogous to covariance between traits
within a single genome. He also emphasizes the role
of epistasis across species boundaries, similar to inter-
genomic epistasis (Wade 2007), but curiously leaves
out explicit mention of Hamilton’s theory even
though kinship correlations are important. Wyatt
et al. (2013) use a spatial model with indiscriminate
(random) helping among individuals in a mixed-
species population. They divide fitness into direct and
indirect (kin) components, using a patch model where
individual fitness depends on the presence of a help-
ing allele in the partner species. Wyatt et al. (2013)
find that the potential for coadapted alleles (i.e.,
mutual reinforcement for helping across species
boundaries) can be counteracted by competition
between species (niche overlap). This is analogous to
local competition among relatives eliminating the
benefits of kin selection in highly viscous populations
(Taylor 1994; Queller 1994; West et al. 2002).
Pollinating Seed Predators: A Role for Kin Selection?
In pollinating seed predator mutualisms, a specialized
pollinator deposits pollen onto the stigma of a host
plant while simultaneously laying eggs onto (or into)
the flower of the host. Among these fascinating sys-
tems, the fig–fig wasps and yucca–yucca moth have
been the most extensively explored by researchers
(Bronstein 2001a,b, Herre et al. 1999). In both figs
and yuccas, the offspring of the pollinator eat a subset
of the developing seeds, a cost that the plant balances
against the benefits of receiving pollen from the adult
female. From the host plant’s perspective, more pollen
(i.e., seed set) and fewer eggs (i.e., less seeds eaten by
larvae) is optimal; as a result, host plants have been
shown to abort flowers with lower amounts of pollen
(Huth & Pellmyr 2000; Jander & Herre 2010) or with
higher numbers of eggs laid (Huth & Pellmyr 1994;
Bronstein 2001a).
This balance between pollination and oviposition
can become more complicated when multiple female
pollinators visit the same individual flower (in yucca)
or the same inflorescence (in figs). In yucca plants,
communal oviposition by the moth Tegeticula yucca-
sella has been shown to increase costs to the host
through mechanical ovule damage (Marr & Pellmyr
2003). Therefore, additional ‘secondary’ pollinators
are unlikely to be good for the primary pollinator
unless they deposit large amounts of pollen and low
numbers of eggs. Otherwise, these additional pollina-
tors only increase the risk of flower abortion and, sub-
sequently, offspring mortality for the initial
pollinator. Could kinship among these interacting
yucca moths influence the stability of mutualism with
their host plants? Might these secondary females
adjust their pollen and oviposition in a way that is
altruistic toward the primary female? There is reason
to think that communally ovipositing yucca moths
are kin; siblings pupate together in the soil at a plant’s
base and most pollination by females occurs within
the same yucca plant or on neighboring plants, with
most adults moving no more than 5 meters (Marr
et al. 2000).
Marr et al. (2000) suggest that the risks of flower
abortion due to self-pollination may be outweighed
by the energetic costs to the moth of collecting pollen
from more distant plants. Flower retention increases
quite dramatically with outcrossed pollen in Yucca fila-
mentosa plants (Huth & Pellmyr 2000), suggesting that
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Kin Selection and Interspecific Mutualism A. G. Zink
the costs of dispersal could be balanced against the
benefits of flower retention and offspring survival. On
the other hand, a longer distance of pollen transport
by yucca moths may not be necessary if seed dispersal
is high and neighboring plants exhibit high genetic
diversity. To complicate matters further, the plant’s
‘decision’ to abort a developing fruit may also be
influenced by pollination rates of adjacent flowers
and retention of adjacent fruits (Becerra & Lloyd
1992; Udovic & Aker 1981). This means that localized
moth behavior is likely to have indirect effects on the
success of other females laying eggs throughout the
plant. In addition, when alternative pollinators are
readily available, it is likely that host plants will adapt
their sensitivity to eggs by preferentially aborting
those flowers (Thompson & Cunningham 2002).
Evidence suggests that there is a host marking pher-
omone released by the yucca moth Tegeticula yuccasella
during oviposition and pollination, indicating that lar-
val competition is likely occurring within developing
fruits (Huth & Pellmyr 1999). But can females recog-
nize kin through these pheromones like many other
insect species? If so, it may be females restrict clutch
size when communal oviposition is with kin, thus sta-
bilizing the mutualism by decreasing the probability
of host flower abortion. Similarly, it is possible that
females actively increase levels of pollination in the
presence of kin eggs within a flower. From the female
moth’s perspective, however, pollen is a limited
resource similar to maternal care and females are
expected to titrate this costly investment based on
number of eggs laid. In addition to competition
among larvae for access to seeds, one unexplored pos-
sibility is cannibalism among yucca moth larvae
within the developing fruit (Pierce 1995). In both
cases, any kin-selected benefits of cooperation that
occur among females ovipositing into the flower must
be balanced against competition among kin within
the developing fruit (West et al. 2001).
In contrast to the yucca moth system, female fig
wasps (in the family Agaonidae) collect and carry pol-
len directly from the one inflorescence in which they
developed. Yucca moths can pollinate and lay eggs in
several different flowers, and because their offspring
pupate in the ground (versus within the host’s inflo-
rescence as in fig wasps), there is a disassociation
between host and pollinator genotypes (Herre et al.
1999). This important difference in dispersal mode
may explain the higher tolerance (higher abortion
thresholds) of fig inflorescences with wasp eggs rela-
tive to yucca flowers with moth eggs (Bronstein
2001a). Fig wasps also present an alternative model
for addressing the potential role for kin selection in
pollinating seed predators because dispersal can occur
over several kilometers (Nason et al. 1998). Female
wasps are forced to be extremely choosy (ovipositing
in only one fig) and will often encounter just a few fig
trees of the species for which they are specialized
(within the genus Ficus; Cook and Rasplus 2003).
Male wasps usually die after mating with newly
emerged females inside of a fig; however, the males of
some species disperse and may even transfer pollen in
some circumstances (Moore et al. 2006). It is
unknown if there is sex-biased dispersal or what pro-
portion of fig wasps are local versus long-distance dis-
persers.
As hypothesized above, the evolution of cheating
by pollinating seed predators, which is common in
many plant–pollinator systems (Bronstein 2001b),
may be slower to evolve if such cheating imposes costs
against kin within a flower or inflorescence. Corre-
spondingly, certain plant genotypes that impose
higher sanctions on their pollinators (Bao & Addicott
1998) may evolve to be more mutualistic. Despite
conflicts arising from the positive correlation between
wasp eggs and seeds eaten in fig inflorescences (Herre
& West 1997), positive associations of female wasp
genotypes and pollen genotypes could lead to linkage
disequilibrium of mutualistic alleles across both spe-
cies (Wade 2007; Queller 2014). This intimate pairing
of female wasps with pollen (paternal genotypes) is
contrasted with the novel maternal genotype that
females (and their seed-eating offspring) encounter
after long-distance dispersal (Nason et al. 1998). This
could, in turn, lead to sexual conflict between pater-
nal and maternal fig alleles associated with the mutu-
alism itself (Yu et al. 2008), although the presence of
dioecious figs in some species makes this dynamic
more complicated (Machado et al. 2001; Cook &
Rasplus 2003).
Like yucca moths, fig wasp females experience com-
munal oviposition within the same fig. In some spe-
cies, a fraction of females are pollen-free in the wild,
suggesting that they may rely on the pollen trans-
ported by other females in the same fig (Jander &
Herre 2010). These host trees are more likely to abort
fruit with experimental introduction of pollen-free
wasps, suggesting that they have evolved sanctions to
prevent this form of cheating (Jander & Herre 2010).
Because the entire inflorescence is aborted in figs
rather than individual flowers, cheaters without pol-
len could possibly free ride on pollen deposited by
other females (Jander et al. 2012). Interestingly, in fig
species that commonly receive two foundress wasps
per fig, the first female has been observed to aggres-
sively dominante the second female that enters the fig
Ethology 0 (2015) 1–8 © 2015 Blackwell Verlag GmbH 5
A. G. Zink Kin Selection and Interspecific Mutualism
afterward (Moore & Greeff 2003). In another species,
females become highly aggressive when a second fo-
undress initiates oviposition, resulting in a fight to the
death; in closely related species with single foundress-
es, such aggressive behavior was not observed (Dunn
et al. 2015).
In both fig wasps and yucca moths, Hamilton’s rule
predicts that females will be less likely to cheat by
withholding pollen when they are laying eggs with
kin rather than unrelated females. Similarly, a general
prediction would be that secondary females lay fewer
eggs to reduce competition with kin, decreasing host
flower abortion and larval competition. Fig wasp
females are less likely to exhibit plasticity in these
behaviors given that their entrance into a fig inflores-
cence is a terminal decision, whereas yucca moths are
free to lay eggs in multiple flowers and exhibit
dynamic decision-making for egg number and loca-
tion. Given that the host fig cannot preferentially
abort single flowers but only the entire inflorescence
(Jander et al. 2012), competition and dispersion
among larvae is also likely to feed back into abortion
dynamics. Future detailed studies of these fascinating
systems, particularly in the context of fig wasp and
yucca moth oviposition and pollination behavior, are
likely to shed more light on the possibilities for apply-
ing Hamilton’s theory of kin selection to pollinating
seed predator mutualisms.
Conclusion
During more than fifty years after the original formu-
lation of Hamilton’s theory of kin selection, recent
models have formalized how kin selection may facili-
tate and maintain mutualisms between species. These
predictions suggest that research on coevolutionary
dynamics should be expanded to consider the specific
nature of social interactions within the component
species. The specific examples of communal oviposi-
tion and larval competition among pollinating seed
predators were chosen to illustrate this point. In addi-
tion, the models reviewed here reveal that future stu-
dies of social evolution should continue to consider
how interactions with other species may reinforce or
undermine kin selection. For example, while socially
transmitted parasites would likely select for kin avoid-
ance, parasites could also reinforce cooperation
among kin if their removal is a social activity. Future
attempts to simultaneously quantify the costs and
benefits of both species interactions and social interac-
tions will open up exciting opportunities for testing
the many predictions of these models.
Acknowledgements
I would like to thank participants in the symposium
on ‘Cooperation within and between species’ at the
2014 International Society of Behavioral Ecology
meeting, Hunter College, NY. In particular, Judie
Bronstein, Kern Reeve, and Kevin Foster provided
feedback on some of the ideas presented here. Mark
Hauber and three anonymous reviewers also provided
excellent and helpful suggestions for improving the
paper. The author was supported by Grant number
IOS-1258133 from the National Science Foundation
and a sabbatical award from San Francisco State Uni-
versity during the writing of this manuscript.
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