David C. Queller

ESTIMATING RELATEDNESS USING GENETIC MARKERS

A new method is described for estimating genetic relatedness from genetic markers such as protein polymorphisms. It is based on Grafens (1985) relatedness coefficient and is most easily interpreted in terms of identity by descent rather than as a genetic regression. It has several advantages over methods currently in use: it eliminates a downward bias for small sample sizes; it improves estimation of relatedness for subsets of population samples; and it allows estimation of relatedness for a single group or for a single pair of individuals. Individual estimates of relatedness tend to be highly variable but, in aggregate, can still be very useful as data for nonparametric tests. Such tests allow testing for differences in relatedness between two samples or for correlating individual relatedness values with another variable.

Microsatellites and kinship

Many evolutionary studies, particularly kinship studies, have been limited by the availability of segregating genetic marker loci. Microsatellites promise to alleviate these problems. Microsatellite loci are segments of DNA with very short sequence motifs repeated in tandem; their often numerous alleles differ in the number of these repeat units. They are very common in eukaryotic DNA and can be amplified by the polymerase chain reaction, which allows the use of minute or degraded DNA samples. The alleles can be scored consistently and compared unambiguously, even across different gels.

Computer software for performing likelihood tests of pedigree relationship using genetic markers

Molecular techniques are making ever more genetic markers available for use in parentage assignment, and measures of relatedness. We present a program, Kinship, designed to use likelihood techniques to test for any non‐inbred pedigree relationship between pairs of individuals, using single‐locus codominant genetic markers. Kinship calculates the likelihood that each pair of individuals in a data set are related by a given pedigree hypothesis, and likelihood ratios for any pair of hypotheses. The program also uses a simulation routine to attach statistical significance to its results.

KIN SELECTION AND SOCIAL INSECTS

Social insects so dominate many terrestrial habitats (Wilson 1990) that they can hardly escape the attention of biologists, but even if they were rare, they would still attract special interest because of the intricate cooperation within their societies. William Morton Wheeler (1911) described the social insect colony as an organism (or as a higher-level organism or superorganism) because of the degree to which individuals appear to operate as a unit that is dedicated to the perpetuation and reproduction of the colony as a whole. The reinvention of the organism at a higher level has occurred at a number of crucial junctures in the history of life (Maynard Smith and Szathmary 1995). For example, the eukaryotic cell arose from several prokaryotic ancestors (Margulis 1970), and multicellular plants, animals, and fungi arose from single-celled ancestors (Buss 1987). Because insect societies are macroscopic, and because they span the entire range from solitary individuals to essentially superorganismal colonies, they offer an accessible model for how such transitions can happen.

Genetic relatedness in viscous populations

SummaryHamiltons inclusive fitness rule shows that the evolution of altruism is facilitated by high genetic relatedness of altruists to their beneficiaries. But the evolution of altruism is inhibited when the beneficiaries are also close competitors of the altruist, as will often be true in structured or viscous populations. However, Hamiltons rule still gives the correct condition for the evolution of altruism if relatedness is measured with respect to the local competitive neighbourhood.

QUANTITATIVE GENETICS, INCLUSIVE FITNESS, AND GROUP SELECTION

Inclusive-fitness models have been criticized because they give incorrect results for cases in which fitness components interact nonadditively. However, this failure is not due to anything intrinsic to the inclusive-fitness viewpoint. It stems from an essentially quantitative genetic feature of the model, an attempt to separate fitness terms from genetic terms. A general rule is provided for determining when such a separation is justified. This rule is used to show how Prices covariance equation is related to standard quantitative genetic results and to derive quantitative genetic equations for inclusive fitness and group selection. It also shows that the group-selection model is no more general than the inclusive-fitness viewpoint. These models serve a role that is different from, but not inferior to, population-genetics models. Although they are less exact under some conditions, like quantitative genetic models in general, they provide us with measurable parameters.

A GENERAL MODEL FOR KIN SELECTION

Inclusive fitness theory is central to our understanding of the evolution of social behavior. By showing the importance of genetic transmission through nondescendent relatives, it helps to explain the evolution of reproductively altruistic behaviors, such as those observed in the social insects. Inclusive fitness thinking is quantified by Hamiltons rule, but Hamiltons rule has often been criticized for being inexact or insufficiently general. Here I show how adopting a genic perspective yields a very general version that remains pleasingly simple and transparent.

Unrelated helpers in a social insect

High-resolution genetic markers have revolutionized our understanding of vertebrate mating systems, but have so far yielded few comparable surprises about kinship in social insects. Here we use microsatellite markers to reveal an unexpected and unique social system in what is probably the best-studied social wasp, Polistes dominulus. Social insect colonies are nearly always composed of close relatives; therefore, non-reproductive helping behaviour can be favoured by kin selection, because the helpers aid reproductives who share their genes. In P. dominulus, however, 35% of foundress nestmates are unrelated and gain no such advantage. The P. dominulus system is unlike all other cases of unrelated social insects, because one individual has nearly complete reproductive dominance over subordinates who could have chosen other reproductive options. The only significant advantage that subordinates obtain is a chance at later reproduction, particularly if the queen dies. Thus, P. dominulus societies are functionally unlike other social insects, but similar to certain vertebrate societies, in which the unrelated helpers gain through inheritance of a territory or a mate.

Detection of highly polymorphic microsatellite loci in a species with little allozyme polymorphism

Microsatellite loci are regions of DNA containing tandem repeats of a short sequence motif; they occur abundantly in all eukaryotic genomes and have been shown to be a rich source of highly polymorphic genetic markers in humans and other mammals. These loci are particularly suitable for population studies because they can be relatively easily scored using a combination of polymerase chain reaction (PCR) amplification of each locus followed by electrophoresis to separate alleles. This paper details a method for finding these loci in any species. This method demonstrates that trinucleotide microsatellite loci are abundant and highly polymorphic in the social wasp Polistes annularis, whereas allozyme electrophoresis reveals very little polymorphism. The first six loci examined were all polymorphic with a mean observed heterozygosity of 0.62; in comparison average heterozygosity of 33 allozymes was 0.035. We suggest that this method can be used to detect variation where other methods have failed, making it an ideal tool for population and conservation geneticists who must deal with populations lacking other types of genetic variability.

Why do females care more than males

Females tend to provide more parental care than males. Previous efforts to account for this have been confused because it is difficult to express the costs of care for males and females in the same currency. Here I propose a null model that does so, using the Fisherian constraint that total male and female reproduction must be equal. The model shows that, contrary to a number of recent analyses, lower probability of parentage for males does tend to make males less likely than females to provide care. It also shows how sexual selection stemming from premating asymmetries in investment promotes similar post–mating asymmetries.