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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: [email protected]

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).

Ethology 0 (2015) 1–8 © 2015 Blackwell Verlag GmbH2

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).


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



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



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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