Behavioral Ecology and Sociobiology

Behav Ecol Sociobiol (1982) 11:223-228

9 Springer-Verlag 1982

On the Evolution of Male Workers in the Hymenoptera Stephen H. Bartz Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts 02138, USA Received May 17, 1982 / Accepted September 24, 1982

Summary. The effects of brood sex-ratio (investment ratio) and the presence of 'laying workers' on relatedness in the Hymenoptera are analyzed. It is shown that the conditions of brood composition that generate degrees of relatedness favorable to the evolution of eusocial type helping behavior among females will select against such helping behavior among males, and vice versa (see Fig. 1). Thus, societies in the Hymenoptera can be expected to have male workers or female workers, but not both. It is argued that the conditions leading to degrees of relatedness favorable to male helping are quite restrictive and unlikely to be met in haplodiploid species. The presence of 'laying workers' is shown to lead to biasses in relatedness such that females may be selected to be workers even when the sex-ratio is male-biassed. This result sheds new light on a possible pathway to eusociality in the Hymenoptera. It is argued that ' offspring parasitism' of the natal nest may have been important in the evolution of eusociality.

Introduction

Trivets and Hare (1976) demonstrated the importance of the sex ratio in creating degrees of relatedness favorable for the evolution of eusocial behavior in the Hymenoptera. They showed that, by itself, haplodiploidy does not make the evolution of eusociality any more likely. When the sex-ratio of broods is 50:50 a female's average degree of relatedness to her siblings is equal to her relatedness to her offspring, and no genetic bias favoring social behavior exists. However, if broods have an excess of females, a female's average relatedness to her siblings exceeds that to her offspring, and selection would tend to favor the evolution of

female workers. In the fol(owing discussion, I extend Trivets and Hare's analysis to examine the potential evolution of male helping behavior. I examine the effects of brood sex-ratio and the presence of'laying workers,' and show that the conditions of brood composition that generate degrees of relatedness that would favor female helpers are precisely those that would select against helping behavior among males, and vice versa. The implications of these findings for the evolution of social behavior in the Hymenoptera are discussed. Results

Evidencefor Male Helping Sterile helpers in colonies of social Hymenoptera species are always female (Oster and Wilson 1978). In spite of the intensive study devoted to the social insects, in only a few instances have males been observed to contribute to colony maintenance. H611dobler (1966) notes that in Camponotus herculeanus and C. ligniperda males live for approximately 1 year in their natal nests. During this time they go through four behavioral phases: social, quiescent, sexual, and senescent. In the first two, especially during the social phase, males engage in trophallaxis with other colony members, both receiving and regurgitating food. They appeared also to help other reproductives emerge from their pupal cocoons. In bees, Houston (1970) reports dimorphic males in a species of the Halictine Lasioglossum. One form is the ordinary sexual type, while the other is wingless and has well developed mandibles that may be suited fior defensive behavior. There are no behavioral observations supporting this possibility, and it seems equally likely that this dimorphism is the result of male - male competition 0340-5443/82/0011/0223/$01.20

224 for mates. A similar situation with two male forms, one winged and the other apterous and heavily armoured, has been reported for fig wasps (Hamilton 1979) and may exist in several ant genera including Cardiocondyla (Santschi 1907) and Hypoponera (LeMasne 1956). In the weaver ant, Oecophylla longinoda, both female and male larvae participate in colony maintenance by producing the silk that is used in nest construction, but the male larvae contribute much less silk than the female larvae (Wilson and H611dobler 1980). For the most part, however, the males of the social Hymenoptera contribute nothing to their natal nests and only sperm to females starting new nests. Hamilton (1964) suggested that the haplodiploid genetics of t h e Hymenoptera cause males to be related less closely to siblings than to offspring, and that the absence of male workers was thus easily understood. Unfortunately, this conclusion was based on a mistake in the calculation of brother - sister relatedness. After correcting this mistake, Hamilton (1972) concluded that he could detect no bias in relatedness, like that existing for females, that would affect the evolution of helping behavior among males. Charnov (1978) concluded that alleles for worker-like behavior among males would be selectively neutral. Recently Craig (1982), modelling the spread of rare alleles causing altruistic behavior, further examined the possibility o f the evolution of male helpers in the Hymenoptera. He, as Hamilton, concludes that the absence of male workers cannot be explained on the basis of biassed degrees of relatedness. The best explanation he says, and one that is favored by Lin and Michener (1972) and Alexander (1974) as well as by Hamilton (1972), is a phylogenetic one: because there is little or no male parental care in solitary nesting Hymenoptera, it is likely that the preadaptations necessary for the evolution of male helping behavior were absent among the ancestors of the modern social species. However, by assuming that females' broods are composed of half daughters and half sons, Craig's analysis neglects the effects of biassed brood sex ratios. When this important variable is considered, a very different picture emerges.

A Brood Composition Model for the Evolution of Helping Behavior The following model analyzes a subsocial pathway to eusociality, like that described by Charnov (1978), in which offspring remain on their natal nests rather than leaving and starting nests of their own. In such a situation, one can imagine the

members of a female's brood faced with two alternative ways of contributing to the production of reproductives: they may either leave their mother's nest, mate and start raising their own offspring on a new nest; or they may remain and help their mother rear more of her offspring. For the sake of the following model several assumptions will be made about the broods of reproductives that individuals produce on their own or on their natal nests. These include: 1. Individuals who remain will help rear a brood composed at least in part of reproductives. 2. All of the reproductive females (alates) will be produced by the original nest foundress (heretofore called' the queen'). 3. The males in the reproductive brood will be from two sources. They may either be queen-laid males, or, if daughters stay and help, some of them may be produced by the queen's daughters. These males are called worker-laid males. 4. Individuals who leave will, if female, mate and start a new nest. They will subsequently produce a brood of reproductives exactly like the one that their mother went on to produce. That is, all nests are identical in brood composition. 5. A male that leaves the natal nest will father a brood just like that subsequently produced on his natal nest. 6. The sex ratio in all broods is the same. It is not assumed, as in other models using a similar life history such as Charnov's (1978) or Aoki and Moody's (1981), that the population sex ratio is at 50:50 and that individual broods' sex ratios are biassed away from the population equilibrium. Rather, I assume that ecological conditions have established a particular sex ratio strategy in the population, and that all broods are composed of the sexes in equilibrium proportions. This view imagines that such factors as local mate competition (Hamilton 1967) or local resource competition (Clark 1978) have resulted in a biassed population sex ratio. It has the advantage that no sex-ratio biassing effects of the altruism alleles need be assumed. 7. All broods are of equal size, and the chance of successfully raising a brood is the same for individuals that stay and individuals that leave. That is, the efficiency with which a worker and a nonhelper can raise an egg to adulthood is the same. Thus, the only difference between an individual's own brood and its mother's brood will be in expected relatedness. The degrees of relatedness that will determine whether an individual will be selected to stay or leave are those of that individual to the reproductives it expects to produce. Thus, as Trivers and

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1/4, 3/8, and 1/2 respectively9 Assuming that a female's own sons will compose an insignificant portion of the group of male reproductives, a female's relatedness to them can be ignored, and only her relatedness to her brothers, sisters, and nephews need be analyzed. As above, the average relatedness, b2, of a staying female to her natal nest's reproductwes as:

1,0

S 0.5

J

.

b) = 3/4 (s) + 1/4 (1 - s) (m) + 3/8 (1 - m) (1 - s)

0

0.5

1.0

m Fig. 1. Brood compositions that would favor the evolution of helping behavior among females are shaded9 Male helping behavior may be favored in broods whose compositions are depicted in the unshaded region. There are no brood compositions for which male and female helping is favored9 s is the proportion of a brood that is female, and m is the proportion of the male reproductives produced by the queen

Hare explained, natural selection will act on the difference between the average relatedness to one's own future reproductive offspring and the average relatedness to the natal colony's reproductives. All else being equal, helping behavior will be favored (alleles for such behavior will spread) when individuals are more closely related to their natal nest's reproductives than to their own offspring9 It should be noted that conclusions drawn from this model are independent of ecological factors that might also favor helping behavior by affecting, not the relatedness of the reproductives produced to the donor of parental care, but rather the number of reproductives produced 9 Looking first at a female's situation, we see that if she leaves and starts her own nest, she expects to produce a brood of reproductives composed of daughters, sons, and grandsons, to whom she is related by 1/2, 1/2, and 1/4 respectively. If s is the proportion of individuals in the brood that are female (assume that males and females cost the same amount of 'investment' to rear), and rn is the proportion of the male reproductives produced by the queen, we can weight the expected proportions of the various kinds of offspring by their respective degrees of relatedness to derive the average relatedness, bl, of this leaving female to her reproductive brood: by= 1/2(s) + 1/2(1 - s ) (m)+ 1/4(1 - s ) (1 - m ) = 1+s+m(1 -s) (1) 4 If she were to stay on the natal nest, she would be raising a brood composed of sisters, brothers, nephews, and sons, to whom she is related by 3/4,

= 3 (1 + s) + m ( s - 1) 8

(2)

Female helping behavior may be expected to evolve when a female is more closely related to her natal nest's reproductives than to her own offspring. This will occur when b'y exceeds by. The values of m and s for which this is true are shaded in Fig. 1. The solid curved line represents the set of9 points for . which b f. and . b'f are equal . . - The equatlon for this curve of indifference is given by: 3m-1 S-3m+a.

(3)

The same analysis can be conducted for males. If a male leaves the nest, he expects to father a brood composed of daughters and grandsons, to whom he is related by 1 and 1/2 respectively9 His average degree of relatedness to this group of reproductives is: bm=

1 + s-m(1

-s)

2

(4)

For a male that stays on the natal nest, the situation is slightly more complex9 Recall that there are two kinds of males: queen-laid and workerlaid9 A queen-laid :male (QLM) expects to be helping to raise a brood of reproductives composed of sisters, brothers, and nephews, to whom he is related by 1/2, 1/2, and 1/4 respectively9 His average relatedness to the nest's reproductives is then: bQLM : 1 + s + m ( l

4

--s)

(5)

A worker-laid male (WLM) expects to be raising a brood composed of aunts, uncles, brothers, and cousins, to whom he is related by 3/4, 1/4, 1/2, and 3/8 respectively. Assuming, as was done for a staying female's sons, that a worker-laid male's brothers comprise an insignificant portion of the reproductive brood, his relatedness to his brothers can be ignored9 The average relatedness of a worker-laid male to his natal nest's reproductives is then: bWLM= 3 (1 + S) + m ( s - 1) 8

(6)

226 Assuming that males cannot tell whether they are worker-laid or queen-laid, to derive the expected relatedness of an average male to the group of reproductives, bQLM and bwLM must be combined, each weighted by the proportion of that type present. The expected average relatedness of a staying male to his natal nest's reproductives is then:

b;. = [bQLd m + [bwL ] (1 - m ) ,

(7)

b' =3(1 + s ) - m [ 2 - 3 m ( 1 - s ) ] (8) " 8 Male helping behavior may be expected to evolve when the value of b~, exceeds that of bin. The values of m and s for which this is true are found in the unshaded region of Fig. 1. Again, the solid curved line indicates the values for which br~ equals b'm" The equation for this indifference curve is: 3m2+2m-1

(9)

S=3m2+4m+ 1" This equation factors to yield ( 3 m - 1) ( m + 1) s = ( 3 m + l ) (re+l)'

(10)

which reduces to

3m--1

S-3m+l-

(11)

Thus, the indifference curves for male-helping and female-helping are the same. The only difference is that, for males, it is the area below the indifference curve that includes the values of m and s for which helping may be expected, whereas for females, it is the area above the curve that indicates favorable conditions for the evolution of helping. Thus, we can draw the major conclusion that the conditions of brood composition that would favor male helping behavior are precisely those that would select against helping females and vice versa. There are no conditions o f m and s, no brood compositions, for which both male and female helping behavior will be favored at the same time. Discussion

The model presented in this paper has at least three important features. The first concerns the matter of the degrees of relatedness that are important in the evolution of social behavior. Lately, the opinion has surfaced that the important degrees of relatedness are those of potential altruists to colony members at large (Wilson and H611dobler 1980). This can be true only in so far as those colony members are reproducing. They may do this by the production of unfertilized, male des-

tined eggs, or by the insertion of an occasional daughter into the reproductive brood. Such production of female reproductives is not, however, expected to be tolerated by other colony members (Trivers and Hare 1976). Relatedness to non-reproductives is simply meaningless, because it is relatedness to individuals who will themselves reproduce that determines whether alleles will spread. The second feature is, of course, the conclusion that male and female helping behavior will evolve under mutually exclusive conditions. Societies in the Hymenoptera are extremely unlikely to have both male and female workers. Although there may be some grains of truth in the argument that male helping in the social Hymenoptera is scarce because males lacked appropriate preadaptations (like, perhaps, a sting), the case is really very weak. In the termites both males and females are included in the sterile castes. There is no good reason to suppose that the males of the prototermite species were any better adapted for domestic activity than the ancestors of the social Hymenoptera species. In addition, the ergatoid males in the ant genera Cardiocondyla, Formicoxenus, and Hypoponera, which are certainly in good position to help, do not appear to contribute anything to colony maintenance. However, ergatoid males almost certainly inbreed, and inbreeding in a possibility not covered in the analysis presented here. It is likely that this model is not strictly applicable to the males in these genera, and a more complex model, incorporating effects of inbreeding, is required to fully analyze selection on ergatoid males. Of the few cases of male participation in colony activities reviewed earlier, one has yet to be confirmed as such, and the other two are special in that males probably incur no great cost to themselves by performing their helpful acts. The model in this paper does not say that male helping behavior should never evolve, it merely states that, all else being equal (i.e. costs and benefits), male and female workers are not to be expected. Certainly, if the benefits were sufficiently large or the costs sufficiently small, male particiaption in colony activities might be expected. In the case of Oecophylla, whose male larvae make silk that is used in nest construction, it seems likely that the costs incurred by these larvae are quite small in comparison with the benefits that their activities confer. Wilson and H611dobler (1980) have shown that these male larvae produce silk at about one tenth the rate of their female counterparts. In addition, because Oecophylla nests may endure long after the death of the queen, and consequently long after

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the production of female larvae has ceased, male larvae may be selected to produce silk in their own reproductive interests (H611dobler and Wilson, in preparation). Concerning the Camponotus species, H611dobler (/964, 1966) has suggested that the short summer season has favored the peculiar life history of these ants that involves a long male tenure in the nest. Because there is very little time for initiating new nests, reproductives must be ready to fly when conditions are good. These species have evolved the habit of keeping adult alates in the nest over the winter to insure that they will not miss the earliest opportunity to fly out and start new nests in the spring. As with Oecophylla, it is likely that the cost to males giving up a little excess food by regurgitation is small compared with the benefits. If the overwintering reproductives had to be fed individually by workers, much more time and energy would be spent maintaining them over the winter. Engaging in what is probably best understood as reciprocally altruistic trophallaxis with other reproductives streamlines the distribution of food and allows for the maintenance of a larger pool of alates. Perhaps there is some cost, in terms of ultimate reproductive success, that the males of these two species are experiencing, but it surely pales in the light of the great sacrifice in personal reproduction made by their sisters. There is simply no well documented case, in any Hymenoptera species, of males sacrificing their own reproduction to aid in colony maintenance or reproduction. That there are no male workers in the Hymenoptera is made more understandable by examining the conditions, specified in Fig. 1, under which male helping behavior may be expected to evolve. The conditions that would lead to degrees of relatedness favorable to male helping are, essentially, broods of reproductives with a consistent excess invested in males. In general, male-biassed investment ratios are rare (Hamilton 1967), and in the Hymenoptera there are few species known to consistently bias brood investment in favor o f males. There are cases, among parasitic species of the Hymenoptera, in which females occasionally produce male-biassed broods, but these same females tend also to produce other broods that are female biassed (Pickering 1980). In addition, honey bees, army ants, and meliponine bees that reproduce by swarming produce very male-biassed broods of reproductives. It is not clear, in these cases, just what constitutes investment in females: are the workers that leave (or stay) with the new queen to be counted as female investment? Among solitary

nesting wasps, such as Philanthus, male-biassed sex-ratios are occasionally produced (Simon Thomas and Poorter 1972). However, when one considers the chance that a daughter might inherit her mother's nest, and the value of the nest is included as some kind of investment in females, the numerically male-biassed sex-ratios appear likely to represent more nearly even investment ratios. It is also difficult to imagine alleles for a malebiassed sex-ratio spreading in a haplodiploid population. Because males have no sons, other alleles in males causing female production would be favored. It is likely that the ancestors of the modern social Hymenoptera were not much different from extant solitary species in their habits of production of the sexes, and consistently male-biassed broods were probably rare. As a third major feature, this model shows explicitly that a female-biassed brood sex-ratio is not essential to create degrees of relatedness congenial to the evolution of eusociality in the Hymenoptera. Trivers and Hare (1976) argue that it is only when broods are consistently female-biassed that females would be more closely related to their siblings than to their offspring. It has thus been subsequently presumed that one of the essential conditions prior to the evolution of eusociality was a female-biassed investment ratio. Factors that might lead to female-biassed sex-ratios, such as local mate competition or bivoltine life history patterns (J. Seger, unpublished), have been implicated in arguments for the evolution of eusociality in the Hymenoptera. Models like Charnov's (1978) assume that the alleles causing helping behavior also possess some kind of sex-ratio biassing effect as well. But, it is only when the queen produces all of the male reproductives that a female-biassed sex-ratio is necessary to create degrees of relatedness favorable to the evolution of female workers. If daughters produce any male reproductives at all, then the requirement for a biassed investment ratio disappears (see also Crozier/977). This is easy to understand intuitively. When a female raises a nephew rather than a brother, she trades a degree of relatedness of 1/4 for one of 3/8. Thus, her average degree of relatedness to a reproductive brood composed of sisters, brothers, and nephews will be greater than her relatedness to a brood composed of only sisters and brothers, and in many instances, greater than her relatedness to the brood she would expect to raise if she started her own nest. Degrees of relatedness favorable to the evolution of female helpers thus need not depend on female-biassed sex-ratios. It is easy to imagine situations in which females return to their natal nests,

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either because they failed to mate or because suitable nest sites are rare and they failed to find a good place to start a new nest. If these females then parasitize their mother's nest by laying a few eggs themselves, the conditions for favorable selection for eusociality will be created. Charnov (1978) has suggested that 'parental parasitism' of offsprings' nests might have been a factor in the evolution of social behavior. I suggest that 'offspring parasitism' of the natal nest might have been much more important in the evolution of eusociality in the Hymenoptera. Acknowledgements. I thank Eric L. Charnov, Nigel R. Franks, Thomas J. Givnish, Bert H611dobler, and Edward O. Wilson for helpful advice and criticism.

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