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Keywords:

  • frequency dependence;
  • genetic diversity;
  • group selection;
  • heterosis;
  • kin selection

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgments
  9. References

Genetic diversity in species is often high in spite of directional selection or strong genetic drift. One resolution to this paradox may be through fitness benefits arising from interactions of genetically diverse individuals. Advantageous phenotypes that are impossible in single individuals (e.g. being simultaneously bold and shy) can be expressed by groups composed of genetically different individuals. Genetic diversity, therefore, can produce mutualistic benefits shared by all group members. We define this effect as ‘social heterosis’, and mathematically demonstrate maintenance of allelic diversity when diverse groups or neighbourhoods are more reproductively successful than homogenous ones. Through social heterosis, genetic diversity persists without: frequency dependence within groups, migration, balancing selection, genetic linkages, overdominance, antagonistic pleiotropy or nonrandom allele assortment. Social heterosis may also offer an alternative evolutionary pathway to cooperation that does not require clustering of related individuals, nepotistic favouritism towards kin, or overt reciprocity.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgments
  9. References

Genetic diversity within species has demonstrable advantages at various levels of biological organization. Heterozygous individuals are often more robust than excessively homozygous individuals (Semel et al., 2006). Social groups function better when genetic variation produces phenotypic variation across individuals in behaviour and morphology (Hölldobler & Wilson, 1990; Robinson, 1992; Cole & Wiernasz, 1999; Mattila & Seeley, 2007). Genetically diverse populations or species can have higher growth rates and be less likely to go extinct (Antonovics, 2003; Reed & Frankham, 2003; Hanski & Saccheri, 2006; Leimu et al., 2006; Vellend, 2006). Nevertheless, the maintenance of genetic diversity is not adequately explained by current evolutionary theory. Natural selection inexorably reduces allelic diversity when better adapted phenotypes are differentially successful in reproduction. Episodes of selective sweeps through populations carry optimal alleles to fixation along with other alleles linked by proximity on chromosomes (Fisher, 1958; Maynard Smith & Haigh, 1974; Kaplan et al., 1989; Falconer & Mackay, 1996; Fay & Wu, 2000). Similarly, genetic drift, especially in small populations, creates stochastic variability that leads to the loss of alleles in populations (Amos & Harwood, 1998; Fay & Wu, 2000). However, the surprising amount of allelic diversity found in many species strongly suggests that directional selection and genetic drift are often significantly opposed (Barton & Turelli, 1989; Turelli & Barton, 2004; Roff & Fairbairn, 2007).

There are a variety of mechanisms by which genetic diversity can be maintained. Some operate through selection at the within-genome level, such as mutation (Turelli & Barton, 2004), heterosis or overdominance (Dobzhansky et al., 1977; Birchler et al., 2006), gene duplication (Lande, 1975; Li et al., 2005), epistasis (Wright, 1931, 1932) and antagonistic pleiotropy (Barton & Turelli, 1989; Curtsinger et al., 1994; Sih et al., 2004; Roff & Fairbairn, 2007). Other processes act across individuals. Most prominent is negative frequency-dependent selection, where the average fitness of an allele in a population declines as it increases in abundance (Maynard Smith, 1982; Olendorf et al., 2006). Multiple alleles can be maintained in the population at evolutionarily stable state (ESS) frequencies when they have equal mean fitness. Populational epistasis can also maintain diversity within and among populations by the creation of multiple adaptive peaks through the fitness effects of interacting traits (Brodie, 1992, 2000; Phillips et al., 2000).

Other mechanisms act across populations either in time or space. Migration between populations under different selective pressures can keep alleles from becoming fixed in any population (Sih et al., 2004; Hedrick, 2005). Varying environmental conditions can also maintain genetic variation by favouring different alleles at different times (Turelli & Barton, 2004; Roff & Fairbairn, 2007).

All of the above processes can potentially maintain genetic diversity. It is not our intention to rate their importance, except to emphasize that no single mechanism explains the considerable amount of the genetic diversity observed in nature. Our goal is to introduce the concept of ‘social heterosis’ as an additional mechanism for the maintenance of genetic diversity. Social heterosis maintains genetic diversity through a mutualistically advantageous expression of multiple alleles at a single locus across interacting individuals (i.e. the simultaneous expression of as many as 2n alleles for a single trait, where n is the group or neighbourhood size). Fitness benefits of genetic diversity accrue at the individual and group levels. Individuals in genetically heterogeneous groups are predicted to have higher reproductive rates than those in homogeneous groups. Diverse groups would experience more beneficial collective properties than would arise within homogenous groups. These benefits can surface as synergisms of genetic diversity, per se, and not specific to particular allele combinations.

Mechanisms for individual-level fitness benefits

Social heterosis can arise in several ways when genetic differences produce behavioural or morphological differences. More diverse groups may exploit a wider range of resources in ways that produce character displacement and reduce intragroup competition. Relevant examples include brook charr (Salvelinus fontinalis) having a genetically based, trophic polymorphism, where individuals specialize in feeding in the littoral or pelagic zones (Bourke et al., 1997; Sacotte & Magnan, 2006), and colour polymorphisms in birds being more likely to be found in species with wider niche breadths (Galeotti & Rubolini, 2004). If differences in behaviour or colouration reduce niche overlap due to specialized feeding strategies, the neighbourhood and individual-level fitness benefits gained from reduced competition could maintain trait variation through social heterosis. A review of individual specialization across a broad range of taxa found 93 species with intrapopulation individual specialization on resources, with at least 16 known to have a genetic basis (Bolnick et al., 2003).

Mechanisms for group-level fitness benefits

Social heterosis may be particularly important when the optimal phenotype cannot be expressed by any single individual. No one individual can be simultaneously tall and short, bold and shy or fast and slow. Yet within each set of dichotomous traits, each character state may have its own unique advantages. Thus, a group of individuals that display a range of capabilities can create a common skill pool that far surpasses the abilities of any one individual (Giraldeau, 1984). Another significant advantage of genetic diversity within a group is increased parasite and disease resistance (Schmid-Hempel & Crozier, 1999). If we think of interacting individuals as superorganisms (Oster & Wilson, 1978; Wilson & Sober, 1989), then their relative immune function would result from the collective properties of each individual's parasite resistance capabilities.

Phenomena, such as niche overlap reduction, skill pools and enhanced parasite resistance, are benefits that are more likely to accrue in genetically diverse populations. We propose that social heterosis can maintain this diversity in the face of directional selection and genetic drift. To validate this concept, we present a model demonstrating the conditions under which social heterosis can operate.

Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgments
  9. References

The basic premise of social heterosis is that alleles (A and B) have higher fitness in the presence of individuals carrying different alleles than with individuals having like alleles (i.e. WA(B) > WA(A) and WB(A) > WB(B)). In our examples, the relative fitness of allele A never exceeds that of allele B, either when comparing across pure groups or within mixed groups. Thus, WB(B) ≥ WA(A) and WB(A) ≥ WA(B). Under these conditions, we examine two questions: (1) when can A possibly invade a population fixed for B; and (2) how effectively can social heterosis maintain genetic diversity in the face of directional selection and genetic drift? Our model assumes haploid reproduction, such that alleles A and B produce individuals and offspring with phenotypes A and B respectively. Overdominance within individuals is not possible. Our model also addresses the simplest case where reproductive success of groups is determined by the number of alleles present and not by their frequency or identity. We do not consider opportunities for coadaptation between alleles, which has been modelled in other studies (see Wolf & Brodie, 1998). There is no selective benefit for any particular pair of alleles to co-occur in the same group. We examine social heterosis only at a single locus in our model, but evolutionarily it is possible that the process could be acting at multiple loci simultaneously.

In a population fixed for allele B, allele A can potentially invade whenever its average fitness is greater (A > B). If social heterosis benefits B more than A (WB(A) > WA(B)), then A can only invade in populations that are subdivided into groups with varying allele frequencies to form structured demes (Wilson, 1980). Allele A will always decrease within all mixed groups. The fitness of a rare, mutant allele A would exceed the mean fitness of allele B, when:

  • image

where n is the size of the group or neighbourhood that experiences the benefit of social heterosis and N is the number of such groupings in a panmictic population. As N[RIGHTWARDS ARROW]∞, the minimum benefit required through social heterosis for A to invade declines such that WA(B)[RIGHTWARDS ARROW]WB(B). By contrast, the social heterosis benefit to A must increase as group size (n) increases. Thus, with the minimum number of possible groups (N = 2), as n[RIGHTWARDS ARROW]∞, WA(B)[RIGHTWARDS ARROW](WB(B)+WB(A))/2. This latter invasion criterion is based on the assumption that having one A individual allows all B individuals to gain equally through social heterosis. This is plausible in small groups, but as group size gets larger the positive effect of A on B might be diluted across all Bs. This would create within-group frequency dependence where gains through social heterosis would depend both on the number of different alleles present and their proportional representation. Although within-group frequency dependence is biologically realistic, we ignore it in our analysis to demonstrate that social heterosis is possible in the absence of any such benefits. This is a conservative assumption relative to exploring social heterosis effects. Adding within-group frequency dependence would make invasion by A more likely.

In a deterministic situation, A will always invade a subdivided population whenever WA(B) > (WB(B)+WB(A))/2 and despite B having higher fitness than A in mixed groups (WB(A) > WA(B)), in homogeneous groups (WB(B)WA(B)) and alone (WB > WA). In a stochastic world, however, alleles can be lost through genetic drift and other nonselective processes even if they have higher relative fitness (Orr, 2000). Thus, to understand the effect of social heterosis on selection for genetic diversity, we need to understand how it can prevent allele loss through drift.

To do so, we constructed a simple haploid model to track allelic diversity in a population. A population is defined as consisting of N groups, each composed of n individuals. In the first generation, multiple alleles (i = 2–10) are present in equal frequency. If all members of a group are of the same allele type (or individuals are alone), the given fitness of alleles is W1 = 1 and for all other alleles Wi = fs, with fs ≤ 1. This defines allele 1 as always having the highest relative fitness. Social heterosis is expressed when an allele's fitness is higher in the presence of other alleles. Thus for allele 1, W1(a) = 1+y(az−1), where y is a constant for the proportional increment in fitness as allele diversity in the group increases (y = 0.05–0.5). A linear effect (z = 1) from the number of alleles (a) present in the group means that each increase in genetic diversity adds the same proportional benefit. Thus, the benefits of diversity behave similarly to additive genetic variance. If z < 1, then genetic diversity has diminishing fitness returns. If z > 1, then genetic diversity has increasing fitness returns, which mimics nonadditive genetic variance. The fitnesses of all other alleles in genetically diverse groups are relative to the ‘best’ allele, such that Wi(a) = fdW1(a), with fd ≤ 1. Therefore, without social heterosis, directional selection drives the population towards fixation of allele 1, whenever fs or fd < 1.

In this model, pure genetic drift in the absence of selection occurs when fs = fd = 1 and y = 0. These stochastic processes are also present in populations under selection (Orr, 2000). Therefore, we quantify the effects of social heterosis relative to the rate at which a given population is expected to lose genetic diversity through drift. The dynamics of social heterosis are determined by varying: group size (n), population size (N), number of alleles initially present in the population (i), the relative fitness of alleles (fs and fd), and the magnitude of benefit from social heterosis (y and z).

Starting populations were simulated across 1000 generations, with 1000–10 000 replicates of each set of starting conditions. In each generation of our model, the population was filled by randomly drawing alleles from a distribution reflecting the proportional representation of each allele after reproduction in the previous generation. Thus, groups were created through random assortment, which negates any effect of kin structure in this model (Pepper, 2000) and creates a population where the average relatedness between group members is zero. Individuals within groups were allowed to ‘reproduce’ relative to their expected fitness as defined by the values of fs, fd, a, y and z. All the offspring were combined in a common pool and the next generation's population was again randomly drawn from this pool of surviving alleles. This methodology replicates a design by Wade (1976, 1977) used in his classic experiments with Tribolium to measure group-level selection for increased reproductive productivity.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgments
  9. References

Social heterosis can maintain allelic diversity under a wide range of conditions. We start with a base case in which allele 1 has the highest fitness in all groups (fs = fd = 0.95, with i = 3 alleles), population and group sizes are small (N = 30 groups, with n = 4 for each group), and the benefits of heterosis are modest (y = 0.1; z = 1). With these conditions, allelic diversity declines similarly to genetic drift (Fig. 1a–c). Social heterosis strongly counters genetic drift when either the benefits of social heterosis increase in magnitude (Fig. 1a), additional allelic diversity has a nonlinear positive increase (Table 1) or the relative fitness of nonoptimal alleles in heterogeneous groups (fd) increases (Fig. 1b). Genetic drift becomes weaker as population size (N) increases. Thus, higher levels of allelic diversity are maintained as social heterosis more effectively counteracts drift (Fig. 1c). The strength of social heterosis is moderately affected by changes in the relative fitness of alleles when alone or in homogeneous groups (fs) and by changes in the number of alleles (i) initially present (Table 1). If we assume all alleles have equal fitness within genetically diverse groups, then even small benefits from social heterosis can counteract genetic drift and maintain high allelic diversity (Fig. 1d).

image

Figure 1.  Social heterosis vs. genetic drift and the loss of allelic diversity over time. In all panels, genetic drift of neutral alleles (with y = 0 and fs = fd = 1) is given by the heavy lines, whereas social heterosis is shown by the thin lines (with fs = fd = 0.95, y = 0.1, z = 1, n = 4, N = 30, and three alleles at equal frequency in generation 0 in all panels, unless otherwise noted). In A, the benefit of genetic diversity (y) is varied from 0.1 to 0.5 per added allele in groups. In B, the proportional fitness of suboptimal alleles within groups relative to best allele (fd) is varied from 0.5 to 1. In C, the number of groups (N) is varied from 30 to 240. In D, the population starts with 10 alleles at equal frequency and with fd = 1, and y is varied from 0.1 to 0.5.

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Table 1.   Results from the social heterosis simulations.
 Mean number of alleles in generation:
2505007501000
  1. For genetic drift of neutral alleles, y = 0 and fs = fd = 1. Social heterosis is simulated with fs = fd = 0.95, y = 0.1, z = 1, n = 4, N = 30, and three alleles at equal frequency in generation 0, unless specifically noted otherwise.

Genetic drift1.2591.0301.0041.001
Fitness in homogeneous groups (fs, with y = 0.2)
 0.102.0601.6201.3831.246
 0.502.1271.6731.4551.308
 0.752.1611.7651.5391.397
 0.952.1661.7721.5691.424
 1.002.1881.8301.6211.458
Nonlinear fitness returns (z)
 0.501.011111
 0.751.0771.0061.0021.001
 1.001.2481.0251.0041.002
 1.251.6691.2051.0711.022
 1.502.2351.7951.4711.304
 1.752.7472.4972.2742.113
 2.002.9532.8822.8212.760
Different number of alleles at generation 0
 2 (w. heterosis)1.4431.1741.0691.020
  (w. drift)1.1861.0221.0011
 4 (w. heterosis)1.8701.3391.1371.054
  (w. drift)1.2671.0371.0031
 6 (w. heterosis)2.0901.4421.2021.110
  (w. drift)1.2911.0261.0051
 8 (w. heterosis)2.1711.4891.2521.172
  (w. drift)1.3281.0381.0041.001
 10 (w. heterosis)2.3211.6271.4101.303
  (w. drift)1.3561.0471.0081.004

The effect of group size on social heterosis is more complex (Fig. 2). Allelic diversity (when starting with i = 6) is best maintained with group sizes of three to six individuals, and the group size in which social heterosis is most powerful increases as the benefits become larger or positively nonlinear. These results follow from the constraints that small groups cannot attain high allelic diversity with only a few group members (maximum a < i). By contrast, larger groups will tend to have low across-group variance in allelic diversity when they are formed randomly across each generation. This increases the relative effects of within-group selection, because the effects of social heterosis will be similar across groups.

image

Figure 2.  The effect of group size on social heterosis. In all panels, fs =fd = 0.95, N = 120/n, and six alleles are at equal frequency in generation 0. The mean number of alleles is given for each 250 generations as group size (n) is varied from 2 to 12. Values of y and z are varied across panels a–c.

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Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgments
  9. References

A central question in evolutionary biology is how population genetic diversity is maintained in the face of many well-documented processes that reduce it (Barton & Turelli, 1989; Turelli & Barton, 2004). Allele loss can result from selection that directly increases individual survival, allele survival (meiotic drive), the reproductive success of genetic kin or sexual selection that increases mating success. Also, demographic processes (e.g. population bottlenecks and genetic drift) can decrease genetic diversity (Amos & Harwood, 1998; Fay & Wu, 2000). Yet, a surprising number of traits retain high allelic diversity (Barton & Turelli, 1989; Roff & Fairbairn, 2007).

We propose that social heterosis is a potentially powerful agent of natural selection for maintaining genetic diversity. Its key element is the positive effect of genetic diversity across individuals to the mutualistic benefit of all. This favours rare alleles in any neighbourhood of interacting individuals. Our results show that genetic diversity can be maintained through social heterosis in the absence of any of the following factors: (1) migration between populations; (2) mutation reintroducing lost alleles; (3) balancing selection favouring different alleles across changing environments; (4) genetic linkages and hitchhiking; (5) overdominance at individual gene loci; (6) coadaptation across alleles or epistasis across loci within a genome; (7) population extinction and recolonization; (8) antagonistic pleiotropy; (9) positive or negative assortment of alleles; or (10) multigenerational associations of groups. Obviously, any or all of the above factors could be simultaneously present and social heterosis may not be the most important evolutionary mechanism for maintaining genetic diversity. Nevertheless, the premise of social heterosis is attractive because it is simple and requires few ecological or genetic assumptions to work.

Our basic model of social heterosis incorporates conceptual elements of single-locus heterosis (overdominance), group-level selection and frequency-dependent selection, but differs from how these have been previously characterized or combined. It is important to make these distinctions clear and to be able to recognize the genetic patterns that would indicate evolution through social heterosis.

Social heterosis and overdominance

Overdominance is expressed at a gene locus when a heterozygote has higher fitness than either homozygote (Birchler et al., 2006). Thus, a person heterozygous for sickle-cell anaemia in a malarial habitat can do better than a person homozygous for the normal allele. The frequency of the sickling allele in the population will depend on the advantage of heterozygosity relative to homozygous normal, and the fitness costs of being homozygous for the sickling allele. Similarly, a heterogeneous group of two may do better through social heterosis than a homogenous group. A key difference, however, is that in a heterozygous individual both alleles will have equal fitness (i.e. gametes will represent equal proportions of the sickle and normal alleles). This need not be true in the heterogeneous group where each individual may have differential reproductive success. If this is the case, a group-structured population is necessary to select for genetic diversity. Classic heterosis at the intragenomic level is independent of population structure (Semel et al., 2006).

A second difference is that social heterosis can produce a complex fitness effect that varies with group size, the number of alleles in the population and the gain function for genetic diversity benefits (Figs 1 and 2). By contrast, classic heterosis does not scale beyond the simultaneous interaction of two alleles.

Social heterosis and trait-group selection

Trait-group models of group selection are generally applied to questions of how beneficial traits can evolve when they impose relative costs on bearers of the trait (Wilson, 1980, 1990). An allele (A) stimulates its bearer to provide a group benefit. The effect of allele A is ‘whole-group’ if individual A also benefits from its own actions, and ‘other-only’ if A benefits those around it but not itself (Pepper, 2000). Whole-group effects function more as mutualisms than altruisms, as all group members are expected to benefit at some level. If these benefits are unequally shared, however, genetic diversity within groups is expected to decline. Whichever allele receives the greatest proportional benefit would eventually displace all other alleles (Wilson, 1980, 1990; Pepper, 2000). Other-only effects are altruistic in the sense that the actor experiences lowered direct fitness to provide a group benefit. Therefore, such a trait can only be selected if genotypes show positive assortment across groups. We do not imply that social heterosis can maintain alleles with other-only effects, and our discussion will be limited to its role in the maintenance of alleles with whole-group effects.

Social heterosis is, by definition, a whole-group effect. Individuals that do not provide benefits (e.g. they have allele B) share any benefits produced by other genotypes, but without any cost of producing it. Therefore, in mixed groups of As and Bs, nonproducers always have higher fitness (Fig. 3: WB(A) > WA(B)). A whole-group beneficial trait can invade a population only when A > B. Because this condition can never exist within a group, the population must be a structured deme where allele frequencies vary across groups. However, it is unnecessary for the population to be composed of clearly defined groups. It can be a single, contiguous population that has local neighbourhoods, as long as the neighbourhoods are heterogeneous and vary in allele frequencies. No special process has to be invoked to create a structured deme as it will arise from random distributions of genotypes (Wilson, 1980, 1990).

image

Figure 3.  Comparison of the group-level dynamics of Wilson's structured deme, frequency-dependent and social heterosis models. The structured deme model assumes an allele providing benefits (A) always improves group productivity, but is at a disadvantage within groups relative to a nonprovider (B). Frequency dependence predicts a rare allele advantage within groups. Selection within groups increases the rarer allele until both alleles have equal average fitness across the population. In social heterosis, an allele's relative fitness is unaffected by its frequency within groups. When comparing homogeneous groups, either WB(B) > WA(A) or WB(B) = WA(A). Similarly, within mixed groups, either WB(A) > WA(B) or WB(A) = WA(B).

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Similar to previous trait-group models, social heterosis also requires a structured deme population where alleles vary in frequency across groups, but it differs from classic trait-group selection in four key ways. (1) Within mixed groups, all alleles can have equal fitness (Fig. 3). The benefit provided need not impose a relative cost to the provider. (2) All alleles have presence/absence effects on group productivity, but their relative frequencies have no effect. By contrast, previous trait-group models have assumed that group productivity always positively correlates with the frequency of the provider genotype. This creates a key evolutionary difference. Pepper (2000) showed that selection for whole-group traits can occur with random or negative assortment across groups (i.e. groups are no more likely or are even less likely to contain related individuals than a random sample of the population). However, positive kin assortment increases the likelihood that previously proposed whole-group traits would increase in frequency. By contrast, because positive assortment decreases within-group genetic variability, grouping with close kin would work against social heterosis. (3) An allele's fitness is always lower in genetically homogenous groups than in heterogeneous groups with social heterosis. Therefore, all group members experience a net benefit from an increase in genetic diversity. These benefits can accrue from actions that are selfish in intent (e.g. foraging in a different manner from others in the group, and thereby reducing within-group competition). Sachs et al. (2004) describe this as a two-way by-product mutualism. By-product mutualism means that social heterosis may be detectable only at a population level, because a given allele can have lower fitness when compared within mixed groups (WB(A) > WA(B)), and when compared across homogeneous groups (WB(B) > WA(A)). Allele fitnesses may only be equal when measured across all groups. (4) The first three differences in the models create the final difference. In Wilson's original model (Wilson, 1980, 1990), the larger the whole-group benefits of the invading allele, the more likely it is to go to fixation. Therefore, this version of a trait-group model would not always maintain genetic diversity in populations. By contrast, larger whole-group benefits serve to maintain multiple alleles in populations with social heterosis (Fig. 1).

Social heterosis enriches and extends the theory of trait-group models. Consider, for example, a situation where neither within-group frequency dependence nor fitness differences across homogeneous groups occur. A traditional view of trait-group models would suggest group-level selection is unimportant in this case. Social heterosis, however, provides an overlooked explanation for how selection occurs at the group level when classical conditions of trait-group models are not met.

Social heterosis and frequency dependence

Frequency-dependent models require that both WB(A) > WA(B) and WB(A) < WA(B) must occur across groups differing in proportions of A and B individuals (Fig. 3). The relative fitness of alleles decreases as they become proportionally more common within groups (e.g. as in Hawk–Dove games; Maynard Smith, 1982). Frequency dependence is necessary for social heterosis, but only as an across-group phenomenon rather than a within-group one. In a randomly distributed population, rare alleles will be in genetically diverse neighbourhoods or groups because they are unlikely to be near other alleles like themselves. Therefore, most rare alleles will experience a whole-group benefit of diversity, but few common alleles will. Averaging across an entire panmictic population, an invading A allele can increase in frequency whenever the invasion criterion is exceeded. This can be true even when WB(A) > WA(B) in the immediate vicinity of phenotype A (i.e. B always does better than A in mixed groups or diverse neighbourhoods).

Social heterosis, therefore, extends the concept of negative frequency dependence to include across-group selection. The implications are most evident when considering how studies currently attempt to demonstrate negative frequency dependence. For example, finding that an allele's relative fitness in groups is unaffected by its frequency, or that a given allele always has lower relative fitness in heterogeneous groups could lead the investigator to reject negative frequency dependence as a mechanism maintaining genetic diversity. However, social heterosis can maintain allelic diversity under conditions not considered by the classic view of negative frequency-dependent selection.

Frequency dependence often arises from alleles interacting in game contexts (Maynard Smith, 1982), and those types of games that favour multiple coexisting strategies can be synergistic with social heterosis. Social heterosis, however, can work without game dynamics. The benefits A and B accrue from each other need not require strategies that produce mutual reciprocity through facultative behaviour (Fig. 3). Therefore, the maintenance of genetic diversity is not dependent on defending against cheaters by either recognizing phenotypic ‘tags’ of others (Axelrod et al., 2004), being clustered spatially together (Doebeli & Hauert, 2005), forming stable groups for multiple generations (Fletcher & Zwick, 2004) or having effective strategies for punishing defection and rewarding cooperation (Taylor & Day, 2004). With social heterosis, alleles can have only effects and not tactics.

Finding evidence of social heterosis

Strong directional selection favouring particular alleles will result in population-wide selective sweeps (Fisher, 1958; Maynard Smith & Haigh, 1974; Kaplan et al., 1989; Falconer & Mackay, 1996; Fay & Wu, 2000). The genetic signatures of selective sweeps are regions of low allelic diversity on chromosomes (Fig. 4). Neutral regions surrounding the selected gene are also swept towards fixation by hitchhiking through linkage disequilibrium (Maynard Smith & Haigh, 1974). The magnitude of the entire region of low diversity depends on how recently the sweep occurred, the strength of selection, and the recombination rate near the selected gene locus (Kaplan et al., 1989; Andolfatto, 2001).

image

Figure 4.  Predicted nucleotide diversity in a region of DNA in a population after a gene locus experiences a selective sweep or selection through social heterosis.

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Therefore, when Hambuch & Lacey (2002) found significantly lower genetic diversity across a number of microsatellite markers in a social tuco-tuco (a fossorial South American rodent) relative to a solitary tuco-tuco species, they inferred strong kin selection and selective sweeps on neutral alleles. By contrast, a major histocompatibility complex (MHC) locus is equally variable in both species. Thus, they further concluded that some other selective mechanism must oppose kin selection and prevent the loss of alleles at these loci in the social species. This pattern of variability is consistent with social heterosis which favours genetic diversity and higher than expected nucleotide diversity (Fig. 4). (It is interesting to note that the current paradigms of evolution for genetic diversity through balancing or frequency-dependent selection do poorly in explaining overall patterns of MHC allelic diversity and distribution across populations; Piertney & Oliver, 2006.) Peaks produced by social heterosis should be narrower than the breadth of selective sweep valleys because allele loss and fixation is prevented. Therefore, neutral regions surrounding loci under selection would not hitchhike to high frequencies.

Another implication of selective sweeps is that traits with stronger fitness consequences should have lower heritability due to greater loss of allelic diversity (Maynard Smith & Haigh, 1974; Falconer & Mackay, 1996; Fay & Wu, 2000). Observed genetic variability, however, varies unpredictably across species (Amos & Harwood, 1998). Seemingly advantageous traits continue to have significant heritabilities (Palmer & Oldroyd, 2003; Hughes & Boomsma, 2004; Kraus et al., 2005), and traits that are more directly tied to fitness do not have reduced heritability relative to traits that more indirectly affect fitness (Stirling et al., 2002). This apparent contradiction of Fisher's fundamental theorem has often led authors to conclude that either the traits are surprisingly neutral in fitness or are maintained by a fortuitously balanced trade-off of costs and benefits (e.g. Kraus et al., 2005). Significant heritability, however, is entirely consistent with the presence of social heterosis.

Conclusions

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgments
  9. References

Social heterosis functions through mutualistic benefits created by genetic diversity in locally interacting individuals that is stabilized by negative frequency-dependent selection across groups. This process can maintain allelic diversity in the face of both genetic drift and directional selection by reducing within-group competition or creating superorganism groups with attributes that cannot be expressed by single individuals. Potential examples of social heterosis can be found in a broad range of taxa from microbes to humans (Table 2). There are numerous examples of behaviour that creates genetically diverse groups; of genetic diversity improving group functioning; and of genetic diversity correlating with reproductive success. Social heterosis is an intriguing evolutionary mechanism that may be implicated in some or all of these phenomena.

Table 2.   Phenomena that potentially could reflect evolution through social heterosis.
SpeciesD, G, NPositive effects or benefits for:PhenomenonReferences
  1. The level of observed interaction is at either the dyad (D), the social group (G) or neighbourhood (N).

Microbes
 PfNPV virusNReplication rateUp to 24 viral genotypes can co-infect a host, without negative effects. Strains can be more productive when in a mixed infection.Hodgson et al. (2004)
 Polio virusNReplication rateComplimentary positive effects across quasispecies. Selection operates on populations, not individual variants.Vignuzzi et al. (2006)
 Social bacteria (Myxococcus xanthus)NForaging efficiency78 different clones found in a soil plot of 16 × 16 cm2. Selection operates mostly during clonal phase of life history.Vos & Velicer (2006)
Plants
 Rice (Zizania palustris)NGrowth & reproductionPlant size and reproductive output per plant increases with genetic diversity.Lu et al. (2005)
 Gas plants (Dictamus albus)NReproductionGenetic diversity correlates with PCA axes of reproductive traits.Hensen & Wesche (2006)
 Wheat (Triticum aestivum)NPathogen resistanceStripe rust disease was reduced in 27 of 28 stands of mixed genotypes compared to pure standsFinckh & Mundt (1992)
 Arabidopsis thalianaNUnknown20 strains are exceptionally genetically polymorphic at loci that mediate interactions with the environment.Clark et al. (2007)
Insects
 Fruit flies (Drosophila  melanogaster)NReproductive successFemales reared in genetically diverse culture are more productive.Peng et al. (1991)
 Bumble bees  (Bombus terrestris)GDisease resistance and reproductive successGenetically diverse colonies have fewer parasites and lower transmission rates.Shykoff & Schmid-Hempel (1991a,b) and Baer & Schmid-Hempel (1999, 2001)
 Honey bees (Apis mellifera)GDivision of labour, brood viability, disease resistanceGenetically diverse colonies exhibit foraging specializations, lower variance in brood reliability, more parasite and disease resistance and more stable nest homeostasis. Diversity leads to higher fitness as measured by reproductive rate and survival.Oldroyd et al. (1992), Fuchs & Schade (1994), Palmer & Oldroyd (2003), Tarpy (2003), Jones et al. (2004), Tarpy & Seeley (2006), Mattila & Seeley (2007) and Oldroyd & Fewell (2007)
 Ants (Hymenoptera: Formicidae)GParasite resistance, colony growth rates, worker caste diversityGenetically diverse colonies are more resistant to parasites and exhibit higher growth rates. Caste diversity at the species level positively correlates with social systems that increase colony genetic diversity.Cole & Wiernasz (1999), Schmid-Hempel & Crozier (1999), Hughes & Boomsma (2004, 2006),  Wiernasz et al. (2004) and Fjerdingstad & Crozier (2006)
Invertebrates
 Snail (Lymnaea stagnalis)NParasite resistancePopulations with lower genetic variation mature slower and have lower fecundityPuurtinen et al. (2004)
 Spiders (Enoplognatha ovata)NForagingWhitish morph tends to ascend into flowers to hunt, whereas greyish-yellow morph hunts more along the groundGreco & Kevan (1999)
Fish
 15 spine stickleback  (Spinachia spinachia)NUnknownMales steal unrelated eggs and add them to their own nests. These eggs neither attract more females nor are preferentially eaten.Jones et al. (1998), DeWoody et al. (2001) and Ostlund-Nilsson (2002)
 Brook charr (Salvelinus fontinalis)NForagingIndividuals specialize in feeding in littoral or pelagic zones.Bourke et al. (1997) and  Sacotte & Magnan (2006)
 Scale-eating cichlids   (Perissodus microlepsis)NForagingRight- and left-jawed morphs are genetically determined and attack prey fish from different sides.Hori (1993)
 Electric fish (Brienomyrus sp.)NUnknown foraging?Electric discharge patterns differ across fish, independent of sex.Arnegard et al. (2005)
 Minkley's cichlid  (Herichthys minckleyi)NForagingTrophic-level morphs feed in different microhabitats with different feeding behaviours. Fish in mixed morph populations have higher feeding rates.Swanson et al. (2003)
 Brown trout (Salmo trutta)GGrowth rateUnder naturalistic conditions, mixed sibling groups grow faster than single family groups.Greenberg et al. (2002)
Birds
 Ruffs (Philomachus pugnax)DReproductive success (putative)Male morphs are genetically distinct and differ in plumage and behavioural reproductive strategy. Females tend to mate with both male morphs. This may increase their reproductive success if sons of varying morphs cooperate to attract females to courts.Lank et al. (2002)
 Barn owls (Tyto alba)NForagingReddish-brown morphs consume field voles more often, whereas light colour morphs consume more wood mice.Roulin (2004)
 Fantails (Rhipidura fuliginosa)NForgagingPied morphs tend to feed in the canopy, whereas black morphs feed in the ground to shrub layer. Colour morphs are controlled by a single genetic locus.Craig (1972)
 Red-tailed hawks  (Buteo jamaicensis)NForagingLight morphs perch in open areas, whereas dark morphs perch in areas with dense cover.Preston (1980)
 Great tits (Parus major)DParental careReproductive success correlates with degree of personality difference in mated pair.Both et al. (2005)
 Galapagos mockingbirds  (Nesomimus macdonaldi)GParental careCooperatively breeding group productivity negatively correlates with male–male relatedness.I. von Lippke (personal communication)
Mammals
 Tuco-tucos (Rodentia:  Ctenomyidae: Ctenomys)GDisease resistanceMHC loci remain as variable as in solitary congeners, whereas other loci have lost variability (due to selective sweep by kin selection?)Hambuch & Lacey (2002)
 Red-bellied tamarin  (Saguinus labiatus)DVisual acuityMated pairs are nonrandom with respect to colour vision. Dyads exhibit significant allelic diversity.Surridge et al. (2005)
 Capuchins (Cebus capucinus)GForagingColour-blind monkeys capture cryptic insects at a higher rate.Melin et al. (2007)
 Old world monkeys (Primates:   Cercopithecidae)NDisease resistanceTRIM5a regions retain high polymorphism across multiple species. The regions are associated with suppressing retroviruses.Newman et al. (2006)
 Chimpanzees (Pan troglodytes)  and humans (Homo sapiens)GForaging preferenceIndividuals within populations differ in their ability to taste bitter plant compounds.Wooding et al. (2006)
 Humans (H. sapiens)DMate choiceMixed-race composites rated as healthier and more attractive than own-race composites.Rhodes et al. (2005)
 Humans (H. sapiens)DMate choiceBoth sexes prefer T-shirts worn by potential mates that share the fewest MHC alleles.Wedekind & Furi (1997)
 Humans (H. sapiens)GForaging and information acquisitionMultiple genes and alleles are linked to attention-deficit/hyperactivity disorder (ADHD)Williams & Taylor (2006)
 Humans (H. sapiens)GGroup functioningCreativity correlates with a variety of personality traits and mental disorders.Reviewed in Lauronen et al. (2004)

It is also worthwhile to consider social heterosis in the context of the evolution of social behaviour. Social heterosis differs significantly from two other mechanisms that are often implicated in the evolution of cooperation: reciprocity and nepotistic kin selection. Benefits of social heterosis arise through intrinsic advantages of interactions between genetically different individuals. Because no single individual needs to exhibit overt altruism or reciprocity to others, benefits are not vulnerable to being subverted by cheating. Individuals neither need to identify those providing group benefits nor have any ability to punish those that do not.

Social heterosis and nepotistic kin selection differ in predicting the trajectories of social evolution. Positive kin assortment increases the potential for nepotism (Pepper, 2000), and expressed nepotism would create groups of high relatedness and populations with reduced genetic variance (Hambuch & Lacey, 2002; Wilson & Hölldobler, 2005). Interestingly, Wilson & Hölldobler (2005) have recently argued that nepotism is more often a dissolutive force and cannot account for the evolution of eusociality. In support of this hypothesis, they cite a dearth of evidence for high relatedness in primitively social forms (but see Helanterä & Bargum, 2007, for counter examples). Instead, they propose that social evolution usually proceeds through groups of low relatedness and is driven by the benefits of group-level cooperation. Their arguments have been sharply criticized on the basis that kin selection encompasses more than nepotism (Foster et al., 2006, but also see Fletcher et al., 2006), and that their model of a social allele is actually kin selection through a greenbeard effect (Thompson, 2006). Overall, Wilson and Hölldobler's model requires positive assortment of related individuals and hence is difficult to distinguish from nepotistic interactions that favour kin aggregation. Social heterosis, however, resuscitates Wilson and Hölldobler's main argument without the need for specific social alleles. Because social heterosis effects are likely to be strongest in groups of distant kin or unrelated individuals, the requirement for positive assortment of related individuals disappears. Social behaviour evolving in the absence of kin recognition or favouritism becomes distinctly possible for suites of traits that produce whole-group benefits (e.g. foraging specializations). By contrast, traits with other-only benefits (e.g. worker sterility) may require kin nepotism.

Within a social heterosis framework, genetic diversity is a positive trait in and of itself. Diversity thus becomes selectable under a variety of conditions, and this allows us to consider new and different realms of evolutionary pathways and effects. The potential of social heterosis as an evolutionary force remains to be explored.

Acknowledgments

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgments
  9. References

We thank F. Adler, D. Blumstein, S. Gilboa, G. Grether, A. Liebert, J. Seger, T. Wang and anonymous reviewers for many helpful comments on the manuscript. PN was supported by NSF grant IOS-0642085.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgments
  9. References