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Genetic variability, queen number, and polyandry in social hymenoptera.

Polyandry, that is, multiple mating by females with different males, occurs throughout the insects, in both solitary and eusocial species (see Walker 1980; Page and Metcalf 1982; Cole 1983; Page 1986). Because polyandry may shape major structural features of insect societies (Trivers and Hare 1976; Starr 1984; Ross 1986; Woyciechowski and Lomnicki 1987; Ratnieks 1988; Boomsma and Grafen 1990, 1991; Ratnieks and Reeve 1991, 1992), and also because it is not immediately obvious why queens benefit from mating more than once (Sherman et al. 1988), several hypotheses have been put forward to explain the adaptive significance of interspecific variation in mating frequencies by eusocial hymenopteran queens (reviewed by Crozier and Page 1985 and Page 1986; see also Moritz 1985). Crozier and Page (1985) and Page (1986) concluded that only three hypotheses merit further consideration as general explanations for multiple mating in social Hymenoptera. (1) Polyandry increases genetic variation within colonies, allowing an expression of genetically based caste systems that is more complete. (2) Polyandry increases genetic variation within colonies, expanding the range of environmental conditions that a colony can tolerate. (3) Polyandry reduces the variance among colonies in the proportion of each diploid brood that is male. Reduced variance is favored when queen fitness is a concave function of the proportion of a colony's diploid brood that is female (i.e., viable).

More recently Sherman et al. (1988) suggested a new hypothesis, namely (4) that polyandry increases genetic variation within colonies, thereby reducing the likelihood that parasites or pathogens will diminish the worker/defense force to the point of jeopardizing the colony's survival and reproduction (Hamilton 1987). Hypothesis 4 has recently gained some support: in the bumblebee Bombus terrestris, parasite transmission is enhanced by high relatedness among colony members (Shykoff and Schmid-Hempel 1991; but see Schmid-Hempel and Schmid-Hempel 1993).

The disease/pathogen hypothesis is similar to hypotheses 1-3 in that all assert that polyandry is advantageous to queens because of the resultant increase in genetic variability within colonies. We refer to these jointly as the "genetic variation," or, simply, "GV" hypotheses. The GV hypotheses stand jointly as alternatives to other hypotheses, such as that queens mate more than once to ensure a sufficient supply of sperm (Cole 1983; Holldobler and Wilson 1990; but see Crozier and Page 1985) or because female mating frequency is genetically correlated to a selectively favored high male mating frequency [Halliday and Arnold 1987; see Crozier and Page 1985 for other, less plausible, hypotheses].

If the function of multiple mating is primarily to increase intracolonial genetic variability (i.e., one of the GV hypotheses is true) and if mating has costs (such as increased energetic loss or risk of predation or venereal disease; Sherman et al. 1988), one would predict that polyandry should be less frequent among polygynous (multiple-queen) species compared with monogynous (single-queen) species, because in the former relatively high amounts of genetic variability already exist because of the reproduction of multiple (and often not closely related) females (Ross and Fletcher 1985; Holldobler and Wilson 1990; Herbers 1993; Ross 1993). If no correlation exists between mating frequency and number of queens, the four genetic diversity hypotheses (GV 1-4) would be seriously weakened.

Here we show that the GV hypotheses are supported when the frequency of polyandry is compared between monogynous and polygynous ant species. We restricted our comparison to ants because this is the only group with sufficient data on both mating frequencies and queen number for an adequate test of the hypotheses.

MATERIALS AND METHODS

The characteristic number of matings of queens is known for only a few of the more than 8000 named ant species. Page (1986) recently compiled many of the published records; to his list we have added species from other published and unpublished accounts. For most of these species, the exact number of matings, the amount of sperm transferred during each of their matings, and patterns of sperm usage are unknown, thus making impossible exact estimates of effective polyandry. As in previous studies (Crozier and Page 1985; Page 1986) species in which both single and multiple mating by queens had been documented were classified as polyandrous. This decision was based on our primary interest in studying why any multiple mating (even if facultative) has evolved within a species.

We encountered three difficulties in categorizing species as monogynous or polygynous. First, many species are facultatively polygynous, such that monogynous and polygynous colonies both occur often within the same population (Elmes 1987; Ward 1989; Elmes and Keller 1993; Ross 1993). We therefore included only species in which queen number had been surveyed in at least 10 colonies (but see table 1 for a few species in which data were available for fewer than 10 colonies), categorizing as polygynous those species in which at least 25% of the surveyed colonies contained more than one dealate queen. We chose this arbitrary cutoff prior to data analysis (following Frumhoff and Ward 1992) to attribute polygyny to species for which multiple queens per colony is a common rather than an infrequent condition. Second, intraspecific variation in queen number among populations is known to occur in several species (e.g., Ross and Fletcher 1985; Elmes and Keller 1993; Rosengren et al. 1993). For such species, it is important to have data on queen number and number of matings for the same populations. Therefore, when data on queen number were available for several populations, including the number of matings recorded, we used only data on queen number from the population(s) for which data on queen mating frequency were also available. Third, several species in the subfamily Ponerinae have unusual social systems, in which a morphologically distinct queen caste can been replaced by one or more mated workers (Ward 1983; Peeters 1987, 1993). We included these species in our analysis recognizing that "monogyny" and "polygyny" here refers to the number of queens per colony. This choice was based on the fact that the number of matings was recorded only for queens and not workers for these species.

Table 1 lists the 58 species in 24 genera and five subfamilies for which data exist on the number of matings by queens. It was possible to document queen number for 53 of these species.

A central problem for comparative tests of evolutionary hypotheses is to determine the lowest taxonomic level at which the independence of taxa can be safely assumed. Treating each species as an independent variable maximizes sample size but risks comparing congeners that share a common phenotype through a shared phylogeny rather than adaptive convergence, leading to violation of independence assumptions of statistical tests (Felsenstein 1985; Harvey and Pagel 1991). The number of times each character state independently arose could be conservatively estimated through a cladistic analysis (Ridley 1983), TABULAR DATA OMITTED allowing a contingency-table test of the proposed association. However, applying this method requires that the systematics of the group under study be well understood; in ants, the phylogenetic relationships of congeners, as well as genera within tribes, tribes within subfamilies, and sub-families within the family are typically very poorly known (Ward 1989).
TABLE 2. Association between queen number and number of matings among ant
genera. Genera are listed according to the predominant condition among
congeneric species based on data in table 1. The number of monogynous
species/total number of species surveyed per genus are listed parenthetically.

                             Monogynous                  Polygynous

Single mating            Aphaenogaster (1/1)          Iridomyrmex (0/1)
                         Pheidole (1/1)               Leptothorax (1/4)
                         Rhytidoponera (2/2)          Linepithema (0/1)
                                                      Myrmica (1/4)
                                                      Solenopsis (0/3)

Multiple mating          Acromyrmex (1/1)             Formica (1/10)
                         Atta (2/3)
                         Brachymyrmex (1/1)
                         Cataglyphis (1/1)
                         Eciton (1/1)
                         Lasius (3/3)
                         Messor (1/1)
                         Mycocepurus (1/1)
                         Pogonomyrmex (9/9)
                         Prenolepis (1/1)


Few data are available to test at which taxonomic level the independence of number of matings by queens can be safely assumed. Four of the seven genera for which the number of matings is documented for at least three species contain both single and multiple-mating species. Both of the two subfamilies with three or more surveyed genera (the Myrmicinae and Formicinae) include both single and multiple-mating genera. This suggests that, at least for the taxa used here, the number of matings is variable within subfamilies and possibly within genera. Queen number has been shown to be a very plastic trait in ants and apart from a few genera (e.g., Pogonomyrmex and Monomorium), which are uniformly monogynous or polygynous, most genera contain both monogynous and polygynous species (Ross and Carpenter 1990; Frumhoff and Ward 1992). These results, coupled with the widespread variation in queen number among conspecific colonies (Rissing and Pollock 1998; Elmes and Keller 1993; Keller and Ross 1993; Rosengren et al. 1993), support the view that queen number in the ants often may be responsive to ecological conditions (Holldobler and Wilson 1977; Herbers 1986a, 1993; Nonacs 1988; Elmes and Keller 1993).

We used two different methods to minimize the problem of treating species as independent variables in genera in which congeners may exhibit a common phenotype through a shared phylogeny rather than adaptive convergence. First, we considered species as independent points only in genera in which variability in queen number or number of matings was reported. In those genera in which no interspecific variation was detected, we treated each genus, rather than species, as a single independent point. In a second analysis of the data, we used an even more conservative method to assess the relationship between queen number and number of matings by treating each genus, rather than species, as a single independent point. For this analysis, we used the same method as developed by Frumhoff and Ward (1992); each genus was categorized according to its predominant condition, with predominance defined as the queen number (multiple versus single) and number of matings (multiple versus single) of the majority of surveyed congeners [table 2; genera with equal number of monogynous and polygynous (or monoandrous and polyandrous) species were not used for this comparison]. We then tested for an association between these two variables.

The genera Harpagoxenus, Polyergus, and Formica sanguinea, which are obligate social parasites, were not considered in these analyses, because, as in other "dulotic" social parasites, Harpagoxenus, Polyergus, and F. sanguinea colonies consist mostly of workers from other species (slaves); thus, in such species the genetic-diversity benefits of multiple mating, if any, are likely much less important than in free living species.

RESULTS AND DISCUSSION

Only three (Rhytidoponera, Pogonomyrmex, and Lasius) of the nine nonparasitic genera containing at least two species exhibited no variation in queen number or number of matings. Treating these genera as independent variables (rather than species) reveals a significant association between multiple mating and monogyny ([[Chi].sup.2] = 6.65, df = 1, P [is less than] 0.01). Only 4 (24%) of the 17 monogynous species (or genera) were monoandrous, whereas 16 (64%) of the 25 polygynous species (or genera) were monoandrous.

Using only genera as independent points yields similar results, with a significant association between multiple mating and monogyny (table 2; [[Chi].sup.2] = 6.12, df = 1, P = 0.013). Only three (23%) (Aphaenogaster, Pheidole, and Rhytidiponera) of the 13 predominantly monogynous genera were predominantly monoandrous, whereas five (83%) of the six polygynous genera were predominantly monoandrous.

The data for genera also were analyzed using continuous variables to categorize the condition of each genus. For each genus, we determined the proportion of polygynous species, thus assigning them values ranging from 0 to 1 (0 = no polygynous species and 1 = all polygynous species). The same procedure was applied with the number of matings (a value of 0 and 1 indicating, respectively, no and all species being polyandrous). These proportions were then arcsine, square-root transformed (Snedecor and Cochran 1980). Comparison among nonparasitic genera reveals a significant negative correlation between the transformed proportions of polygyny and polyandry (Pearson correlation coefficient r = -0.53; N = 20; P = 0.017).

Four of the 24 genera contained monoandrous and polyandrous as well as monogynous and polygynous species. In the genus Myrmica, there was no clear relationship between queen number and number of matings, with two out of the three polygynous species as well as the monogynous species being monoandrous. It should be mentioned that queen number is an extremely plastic trait in this genus, with all known species exhibiting both monogynous and polygynous colonies (Elmes and Keller 1993). The species listed as being monogynous (Myrmica punctiventris) has also been shown to exhibit polygynous colonies in other populations (Herbers pers. comm. 1993). Among the three other genera, there was an association between queen number and mating frequency. In Atta texana, the only polygynous species in this genus, Moser (1967) concluded from his data on sperm counts that some queens may mate twice. However, the nine newly mated queens Moser collected had the same mean number of sperm (99.8 million) as the mean number of sperm (99.9 million) contained in the seminal vesicles of 16 males, indicating that queens may in fact mate singly. A slightly higher number of sperm was found in queens collected from incipient (1-2 yr old) nests, but these differences may have arisen from year-to-year differences in the number of sperm males possess and transfer during mating. (Such variation has been documented in Linepithema humile (= Iridomyrmex humilis auct.); see Shattuck [1992] for the name change), probably arising from ecological factors affecting the trophic status of the colonies and male size (Keller and Passera unpubl. data). Overall, these results indicate that a single A. texana male generally can fill the queen's spermatheca. This contrasts with the two other monogynous species of this genus in which queens store three to eight times the amount of sperm that a single male possesses. Formica exsecta (the only monogynous species among the 11 Formica species surveyed) is polyandrous, whereas some other polygynous species are monoandrous. Finally, in the genus Leptothorax, the only monogynous species (Leptothorax nylanderi) mates multiply, whereas the three other species are polygynous and mate singly.

Some caution is necessary in interpreting these data. This is because the data base on queen number and mating number is not very reliable. However there is no a priori reason to believe that this may have led to a consistent bias in the estimation of frequency of multiple matings in monogynous versus polygynous species. The only possible bias, which would run counter to the observed trend, results from monoandry being more easily detected in monogynous species by allozymes studies. This is because monoandry can be inferred in monogynous species when the coefficient of relatedness among workers is 0.75, whereas allozyme data do not allow estimates of the number of matings in polygynous species in the absence of data on how many queens reproduce and how they divide up reproduction. (Demonstration of monoandry using allozyme data in polygynous species generally requires keeping queens individually in experimental colonies to determine the genotypes of their daughters; see Ross and Fletcher 1985.)

Three possible causal relationships may account for the association between queen number and number of matings. The number of matings may be influenced by queen number, the number of queens per nest may be influenced by the number of times they mate, or both factors may be influenced by a hidden third factor. Although the second possibility cannot be ruled out, it seems unlikely. Shifts in queen number have been shown to be generally associated with important changes in the life history of ant species, such as mode of colony reproduction (Holldobler and Wilson 1977; Keller 1991, 1993a), intercolonial aggression (Keller and Passera 1989a), reproductive output per queen (Keller 1988; Ross 1988), and the size, physiology, and morphology of female sexuals (Keller and Passera 1989b; Passera and Keller 1990; Keller and Ross 1994). Queen number and these various life-history traits are, in turn, dependent on ecological factors such as nest-site limitation, likelihood for colonies to lose their queens, and relative life span of queens and colonies (Holldobler and Wilson 1977; Herbers 1986a; Keller and Passera 1990; Nonacs 1988, 1993). If increases in queen number were driven by the need to increase genetic diversity in monoandrous species, then we would not expect polygyny to be associated with the abovementioned life-history differences and ecological factors. Of course, it is possible that ecological factors that favor polygyny also independently favor monoandry, but it is unclear why this would be the case.

In conclusion, this survey shows that, as predicted by the GV hypotheses, polyandry is less common among polygynous than among monogynous species. Furthermore, it seems that the causal relationship underlying this association is that the number of matings by queens depends on the number of queens present in the colony (rather than the number of queens being influenced by the number of matings), which also supports the GV hypotheses together with the assumption that mating has costs.

ACKNOWLEDGMENTS

L.K. was supported by the Swiss National Science Foundation grant numbers 823A-0283650, 31-35584.92, and 31-36907.93, and the Janggen-Pohn Stiftung. H.K.R. was supported by a Junior Fellowship from the Harvard University Society of Fellows. For discussion and comments we thank K. Boomsma, A. Bourke, A. Buschinger, N. Carlin, J. Herbers, P. Nonacs, J. Seger, J. Shellman-Reeve, and two anonymous reviewers. S. Cover kindly provided unpublished data on queen number for several species. N. E. Pierce and E. O. Wilson graciously provided us with laboratory space and other assistance.

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NOTE ADDED IN PROOF

An additional hypothesis for the evolution of multiple mating by queens has recently been proposed (Queller 1993; Ratnieks and Boomsma in press; see also Moritz 1985; Pamilo 1991). Boomsma and Grafen (1991) showed that workers can enhance their inclusive fitness by biasing colony sex allocation in response to their queen's mating frequency. At the worker optimum, colonies with queens of higher mating frequency should specialize on male production and colonies with queens of lower mating frequency should specialize on queen production. Empirical evidence for this has been provided by the ant Formica truncorum (Sundstrom 1994). As predicted, colonies headed by singly-mated queens produced mostly queens, whereas colonies headed by multiply-mated queens produced mostly males. Given the occurrence of this facultative worker reproductive strategy, queens may enhance their inclusive fitness by increasing their mating frequency, because the queen-optimum sex-allocation ratio is more male-biased (i.e., 1:1) than is the worker-optimum allocation ratio (see Ratnieks and Boomsma in press). This hypothesis, like the other GV hypotheses, provides a means by which a queen may benefit from increasing her mating frequency. However, in contrast to the other GV hypotheses, it is not genetic diversity per se that is beneficial, but diversity relative to other colonies. As with the other GV hypotheses, this hypothesis predicts that polyandry will be less common among polygynous than among monogynous species, because variation in queen number has a greater effect on relatedness asymmetries than variation in mating frequencies. Therefore, the benefits of multiple mating will be lower in polygynous than in monogynous species because variation in mating frequency of individual queens will frequently have little effect on colony genetic structure, in comparison with variation in queen number. In conclusion, the association between queen number and number of matings is also consistent with the hypothesis that queens enhance their inclusive fitness by mating multiply so as to induce workers to produce males.
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Author:Keller, Laurent; Reeve, Hudson K.
Publication:Evolution
Date:Jun 1, 1994
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