GENE DIVERSITY IN HYMENOPTERA

Hymenopteran species display levels of electrophoretic variation significantly lower than most other insects, and a few of them lack variation altogether. These observations are variably explained by reduced heterozygote advantage, inbreeding, eusociality, environmental stability conferred by the nest microhabitat, facilitation of exposure of deleterious genes in the haploid sex, reproduction by arrhenotokous parthenogenesis with balancing selection, and small effective population size resulting in a reduction in the amount of neutral polymorphism (Suomalainen, 1962; Crozier, 1970; Hartl, 1971, 1972; Snyder, 1974; Metcalf et aI., 1975; Pamilo et aI., 1978a, 1978b; Pamilo and Crozier, 1981; Wagner and Briscoe, 1983). Recently, Berkelhamer (1983) tested several hypotheses concerning the low levels of intraspecific genetic variability in Hymenoptera. Her conclusions were: (I) Hymenopterans have significantly lower variability than other insects due to their haplodiploidy. (2) Primitively eusocial insects are less variable than either solitary or advanced social species, implying that eusociality arises as a consequence of inbreeding. (3) Polygynous and monogynous species have similar levels of variability, challenging the expectations derived from both the neutral theory ofevolution (Kimura, 1968) and Hamilton's (1964) hypothesis. Hamilton's hypothesis is later rescued by assuming that the increased effective population size provided by polygyny is balanced by a more severe regime of inbreeding than in monogynous species. Unfortunately, three major errors and several minor ones in the analysis raise doubts as to the validity of these conclusions. The first error concerns the interchangeable use of observed heterozygosity, Hob, (the average proportion of heterozygous loci per individual) and expected heterozygosity or average gene diversity, Hexp, defined as the mean of h over all loci, where h = I :! : xl, and Xi is the frequency of the ith allele at a locus (Nei, 1975). In her Procedures section, Berkelhamer (1983) claims to have used Hobn but her data contain both Hob' and Hew For example, in the case of Opius juglandis and other species from Lester and Selander (1979), she uses Hexp, whereas, when given a choice between ,Hexp and Hobn as in the case of Rhytidoponera impressa (Ward, 1980), she chooses Hob,. Hob, is very sensitive to the mating structure of a population and the amount of inbreeding. When inbreeding is strong, Hob, can be very low, while Hexp is not affected. In extreme cases such as selfing species (e.g., Selander and Hudson, 1976) Hob, is effectively 0, yet Hexp can be large. We also note that haploid organisms, which, by definition, have Hob' = 0, are among the species with the highest gene diversity (Spieth, 1975; Krzakowa and Szweykowski, 1979; Selander and Levin, 1980; Gaur et al., 1981; Yamazaki, 1981). For comparative purposes, Hexp rather than HOb' should be used as a measure of genetic variability (for further details see Nei, 1975; Nei and Graur, 1984). In Hymenoptera, where mating structure can assume diverse forms, the distinction between HOb' and Hexpis particularly important. While it may be difficult to ascertain which species are inbred, the fact is that, in almost all cases, Hob, is less than Hexp, such that using HOb' will introduce a unidirectional bias. In Heliothis zea, for instance, the difference is 21%. It should be noted that other compilations of protein polymorphism (e.g., Soule, 1976; Nevo, 1978) often include a mixture of Hob' and Hexp. The second problem concerns the number ofloci used to determine gene diversity. In Table 2 of Berkelhamer (1983), 51 hymenopteran species are listed, but the number of loci in the majority of them is very low. Presumably, the same is true for non-hymenopterans. Since genetic diversity is known to have a huge standard error (Nei and Roychoudhury, I974b), it is advisable to use estimates based on at least 20 loci. This is especially true when genetic variability is low. When different groups of species are compared by pooling many species within each group, fewer than 20 loci may be used, provided that we examine the same set ofloci. This stipulation derives from the fact that different loci have different levels of heterozygosity (for reasons see Zouros, 1976; Harris et al., 1977; Koehn and Eanes, 1977, 1978; Ward, 1977; Nei et al., 1978; Turner et aI., 1979). Moreover, since students of genetic diversity tend to study the more polymorphic loci first, using a small number of loci tends to introduce an additional bias in Hexp. This sometimes has dramatic effects on estimates of gene diversity. For example, in humans, estimates of Hexp for blood groups are 0.264, 0.197,0.130, and 0.114 when calculated in chronological order, on the basis of 21, 34, 57, and 67 loci respectively (Nei and Roychoudhury, 1974a, 1982). In the case of Drosophila pseudoobscura, Hexp was estimated to be 0.136 based on 46 loci (Fuerst et aI., 1977), while