944 Animal Behaviour, 36, 3

Full Sisters and Super Sisters: a Terminological Paradigm

During the last 10 years the use of genetic tech- niques for studying the behaviour of social insects has steadily increased. Prior to this time, the study of social genetics was limited primarily to bees. Most early studies emphasized the genetic im- provement of social traits of honey bees, Apis mellifera L., that were of economic importance (Laidlaw & Eckert 1950). Studies of genetic com- ponents of individual and social behaviour were introduced by Rothenbuhler (1960). Hamilton's hypothesis for the evolution of altruism and related phenomena (1964, 1972) resulted in the application of molecular genetics to study the social structure of natural populations (Metcalf & Whitt 1977). Development of improved statistical methods for allozyme data followed and expanded the use of genetic markers into more sophisticated studies with the objective of quantifying the genetic and social structure of populations (Pamilo & Crozier 1982).

Recently, the study of kin recognition in social insects has come to the forefront of sociobiology. Specific mating designs are now being used to control the genetic relationships of interacting individuals (see Page & Breed 1987 for a review). Many studies use discrete or continuous genetic markers to identify the group membership of individuals used in behavioural assays. With con- trolled mating it is necessary to standardize breed- ing terminology used in experimental sociobioiogy. We describe the two systems of terminology that are currently being used and recommend the adoption of the system that is genetically more precise.

There are two different sets of nomenclature, both derived from honey bee breeding, that des- cribe the familial relationships of haplodiploid female siblings. The set used most commonly is based on the apparent physical pairing of indi- viduals (Crow & Roberts 1950); the less commonly used set is based on genetic pairing (Laidlaw & Eckert 1950; Polhemus et al. 1950). According to physical-pairing terminology, males are distinct reproductive individuals that represent one-half of a reproductive generation (Crow & Roberts 1950). Siblings that have the same mother and the same drone father are called full sisters. Siblings that have the same mother but have different drone fathers are called half sisters.

With genetic-pairing terminology, the source of the genomes contained in the gametes of males and females is considered. All matings take place between females, with males serving only to rep- licate and transfer, via their spermatozoa, the

genomes that were derived in females. Males are not members of a distinct reproductive generation but are gametozoons, the animal equivalent of gametophytic plants.

Females are the originators of all genomes in the Hymenoptera (at least until functionally meiotic, diploid males are found). Males replicate the genome several thousand to several million times and reverse the sex of the embodying gametic cell from an egg, which was produced by a female, into a spermatozoon.

Genetic-pairing terminology considers the origin of the genomes involved in the mating, which is the only way that diplodipioid and haplodiploid gene- tic systems can be reconciled. With this paradigm, hymenopteran females act as both male and female reproductives. Siblings that share the same mother and the same replicated genome from a common drone also have the same drone mother in common and are called super sisters. The term super as applied to haplodiploids is consonant with Droso- phila genetics where the term super gene is used to describe groups of genes that are closely linked and inherited as a unit without recombination (see Rieger et al. 1976 for a list of terms using super as a prefix). In this case, super is appropriate because super sisters share a parental genome that is inherited as a unit without recombination. (Some Drosophila geneticists now prefer the prefix meta, see Rieger et al. 1976, page 354.) In the absence of inbreeding, super sisters share an average of three-quarters of their genes by common descent (Table I).

Full-sister diploids each come from two different genomes, one derived from the mother and one from the father. The genomes of each parent are products of recombination (except for sex-linked genes) and are not inherited as a unit. On average they share one-half of their genes because of common descent.

Full-sister haplodiploids can be defined in the same way as full-sister dipioids: they come from two different genomes of a common mother and from two different genomes of a common father. In this case the father is the female that originated the genomes of the males. The two different genomes were carried by two different drones that were gametozoons of a single female. The average genetic relationship of full-sister haplodiploids is one-half, the same as for diploids.

With the genetic-pairing terminology, maternal half sisters are defined in the same way for both diploids and haplodiploids. They share the same mother, each receiving a different genome from her. The other genome for each comes from different drones derived by parthenogenesis from different females.

Short Communications 945

Table I. Relationships of individuals discussed in the text comparing physical- and genetic- pairing terminology

Physical- Genetic- pairing pairing Diploid

terminology terminology equivalent* a t

Full sister S Super sister None 0.75

None Full sister Full sister 0.50

Paternal Super half sister:~ half sister None 0.50

Cousins:~ Paternal Paternal half sister half sister 0-25

Maternal Maternal Maternal half sister half sister half sister 0.25

clearly distinguishes all relationships and is effi- cient because it is completely concordant with existing diploid terminology. Physical-pairing terminology is neither sufficient nor concordant and does not account for the unique relationships among hapiodipioid individuals. Therefore, we propose the universal adoption of genetic-pairing terminology. The identical genomes derived from parthenogenetic males represent a unique charac- teristic of haplodiploidy and are responsible for many of the characteristics o f hymenopteran gene- tics that interest sociobiologists: they deserve spe- cial recognition.

We thank Sydney Cameron, James Crow, Ross Crozier, Gene Robinson and Dana Wrensch for their comments about this manuscript.

* Terminology used for diploid genetics that is equivalent to the haplodiploid case.

t G is the pedigree coefficient of relationship (Pamilo & Crozier 1982), assuming standard Hardy-Weinberg conditions.

:~ Terminology that is genetically inconsistent with existing diploid terminology.

Paternal half sisters have different mothers but can share a common father in two ways: (1) sisters share a common drone mother but are derived from different genomes (drones) from her; or (2) sisters share a common genome transmitted by the same drone. Hal f sisters of the first type are genetically equivalent to paternal half sisters of diploids and on average share one-fourth of their genes in common. Paternal half sisters o f type 2, however, are again unique to haplodiploids. On average, they share one-half of their genes in common, due to common descent, as do full-sister diploids and haplodiploids. We propose that these half sisters be called super half sisters in order to recognize the inheritance of identical genomes from the paternal parent.

Super half sisters deserve a status distinct from other half sisters because of the increased propor- tion of shared genes. They likewise deserve distinc- tion from full sisters because of the variance in the proport ion of shared genes. Like full sisters, super half sisters share on average one allele in common at each gene locus as a consequence o f common descent. However, unlike full sisters, super half sisters always share exactly one allele, whereas pairs of full sisters can share zero, one, or two alleles per locus. This difference in variance could be very important for genetic and behavioural studies.

The need for concise terminology is apparent. Genetic-pairing terminology is sufficient because it

ROBERT E. PAGE, JR* HARRY H. LAIDLAW, JRt

* Department of Entomology, Ohio State University, Columbus, Ohio 43210, U.S.A.

t Department of Entomology, University o f California, Davis, California 95616, U.S.A.

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(Received 17 October 1987; revised 12 November 1987; MS. number: As-500)