Social breeding

In some species, helpers may assist breeding adults to raise their young, and this creates a system that is known as social breeding. There are several categories of social breeding, the most developed of which is found in eusocial species. These are characterized by a division of labour that results in numerous workers assisting relatively few reproductive nest mates to raise their offspring. In most cases these workers will never reproduce themselves, often because they are sterile. Most eusocial species are insects, including termites, ants and some species of wasps, bees, aphids and thrips. Eusociality in other orders is very rare, with two notable exceptions being the snapping shrimp (Synalpheus regalis) and several species of naked mole rat (Heterocephalus glaber and Cryptomys spp.). Less stringent forms of sociality involve helpers that may reproduce in later years, and can be found in diverse taxa including about 3 per cent of bird species (e.g. the white-throated magpie-jay, Calocitta formosa), a number of mammalian species (e.g. meerkats, Suricata suricatta) and multiple fish species (e.g. cichlids, Neolamprologus brichardi).

From an evolutionary perspective, scientists have long debated why individuals should invest time and effort in raising young that were clearly not their own. One common explanation for this behaviour is kin selection, which refers to the indirect benefits that an individual can accrue by helping its relatives (and therefore some of its genes) to reproduce. Kin selection is based on the concept of inclusive fitness, which is a fitness value that reflects the extent to which an individual's genetic material is transferred from one generation to the next, either through its own offspring or through the offspring of its relatives.

Kin selection was first proposed by Hamilton (1964), who suggested that an altruistic trait such as helping at the nest will be favoured if the benefits (b) of this trait, weighted by the relationship (r) between the helpers and the recipients, exceed the costs (c) to the helper, because under these conditions an individual's alleles will proliferate more rapidly under kin selection compared with personal reproduction. This can be expressed as:

If helping at the nest meant that an individual would die before he had produced any offspring, the cost to his fitness would be one (c = 1). If he helped to raise full-siblings, then the relatedness between the helper and the chicks would be 0.5 (r = 0.5; Box 6.3). If kin selection was the driving force, this altruistic behaviour would be favoured only if it meant that more than two full-siblings would survive, because (0.5)(2) = 1, but (0.5)(3)>1. Hamilton is said to have worked out this rule in the pub one night, when he claimed that he would lay down his life for more than two siblings or eight cousins, a statement that can be understood in light of the relatedness values that are given in Table 6.3.

Table 6.3 Some coefficients of relatedness in diploid species. Two individuals that have a relatedness coefficient of 0.5 will have 50 per cent of their alleles in common

Coefficient of relatedness (r) Examples

1.0 Identical twins

0.50 Parents and offspring

Full-siblings (both parents in common) 0.25 Grandparents and grandchildren

Aunts/uncles and nieces/nephews Half-siblings (one parent in common) 0.125 Cousins

Great grandparents and great grandchildren

6.3 Estimating relatedness from molecular data

The genetic relationships between individuals are usually referred to as r, the coefficient of relatedness, some examples of which are given in Table 6.3. Relatedness refers to the proportion of alleles that two relatives are expected to share, i.e. the probability that an allele found in an individual will also be present in that individual's parent, sibling, cousin, and so on. In a sexual diploid species, the coefficient of relatedness between parents and offspring is 0.5 because an offspring will inherit half of its DNA from each parent and will therefore share 50 per cent of its alleles with its mother and 50 per cent with its father. After another generation has passed, the new offspring once again has a 50 per cent probability of inheriting an allele from one of its parents, and the likelihood that it has inherited a particular allele from one of its grandparents is (0.5)(0.5) = 0.25, therefore r = 0.25 between grandchildren and grandparents.

The examples shown in Table 6.3 are straightforward but in ecological studies we are more likely to be interested in the relatedness between two individuals for whom we have no prior information, and we cannot estimate this from the total proportion of their shared alleles. We therefore need other methods to estimate the r values of individuals whose relationships are unknown. One approach is to use the frequencies of alleles in individuals and populations to determine whether or not alleles are more likely to be shared because of common descent or because of chance. The more closely related two individuals are to each other, the more likely they are to share alleles because of common descent. If, however, they share only alleles that occur at high frequencies in the population, we may conclude that these alleles are shared simply as a result of chance.

We already know how to estimate population allele frequencies, and the frequency of an allele in a diploid individual must be either 1.0 (homozygote), 0.5 (heterozygote) or 0 (allele absent). Based on this information, the relatedness of one individual to one or more other individuals can be calculated from allele frequency data as:

where for each allele p is the frequency within the population, px is the frequency within the focal individual, and py is the frequency within the individual whose relationship to the focal individual we wish to know. Only those alleles that are found in the focal individual (x) are included in the equation (Queller and Goodnight, 1989). This method is incorporated into the software program 'Relatedness' (see useful websites and software at end of chapter). Note that this equation can generate either positive or negative numbers, with negative values resulting from very low levels of relatedness.

We shall work through this equation using a relatively straightforward example in which we are interested in whether a focal individual (individual x) within a cooperatively breeding group of birds is related to a single female whose brood he is helping to raise. In this example, genotypes are given as the sizes of the amplified microsatellite alleles. The focal individual is homozygous at microsatellite locus 1 (120, 120) and heterozygous at microsatellite locus 2 (116, 118). The potential relative is heterozygous at locus 1 (120, 122) and homozygous at locus 2 (118, 118). When calculating relatedness, we consider only the three alleles that are found in the focal individual (120, 116 and 118). The frequencies used in this calculation are:

Allele

px

py

p

120

1.0

0.5

0.65

116

0.5

0

0.20

118

0.5

1.0

0.35

Relatedness is therefore calculated as:

[(0.5 - 0.65) + (0 - 0.20) + (1 - 0.35)]/[(1 - 0.65) + (0.5 - 0.20)

This suggests that the two birds are quite closely related to each other, although in practice we would interpret this finding with caution because it is based on only two loci, and more data - possibly from up to 30-40 microsatellite loci or >100 SNP loci -- are needed before relatedness coefficients can be calculated with a high degree of confidence (Blouin et al., 1996; Glaubitz, Rhodes and DeWoody, 2003).

Genetic data have enabled us to calculate the relatedness of breeders and their helpers with relative ease (Box 6.3), and these relatedness values have helped biologists to determine whether or not kin selection is a plausible explanation for social breeding. One species in which this seems to be the case is the bell miner (Manorina melanocephala), which breeds within discrete social units that consist of a single breeding pair plus up to 20 helpers. One study found that the majority of these helpers (67 per cent) were closely related (r>0.25) to the breeding pair (Figure 6.8; Conrad et al., 1998). Kin selection may also explain cooperative breeding in the eusocial Damaraland mole-rat (Cryptomys damarensis), in which the mean colony relatedness was found to be r = 0.46 (Burland et al., 2002). In some cases the overall relatedness between helpers and offspring may be reduced by EPFs, for example the moderately high level of EPFs (19 percent of 207 offspring) in western bluebirds (Sialia mexicana) meant that the mean relatedness between chicks and the males that were helping their parents to raise these young was 0.41 (Dickinson and Akre, 1998). This was lower than the relatedness value of 0.5 that is expected if the helpers and chicks were all full-siblings, although the reduction from 0.5 to 0.41 does not necessarily preclude kin selection as a driving force.

Figure 6.8 Genetic similarity between different groups of bell miners (┬▒CI), based on the proportion of shared genetic markers. These data show that helpers at the nest are related to the nestlings. Redrawn from Conrad et al. (1998)

On the other hand, genetic data have shown that fairy-wren helpers (Malurus cyaneus) often assist in the rearing of young to which they are unrelated (Dunn, Cockburn and Mulder, 1995), and male white-browed scrubwrens (Sericornis frontalis) that are unrelated to the breeding female actually are more likely to help raise her young (Magrath and Whittingham, 1997). Social breeding clearly cannot be explained by kin selection in these species and therefore other factors must be taken into account. These may include gaining experience in parental care, increasing the likelihood of being allowed to remain in the colony, or improving the chance of future survival or reproduction. Ecological constraints may also favour social breeding if there is a limited supply of food, nest sites or other resource, and this may explain why socially breeding bird species are relatively common in the environmentally harsh arid and semi-arid regions of Africa and Australia where high quality habitat is in short supply.

Social insects

The previous examples were based on the relatedness values between diploid individuals, but no discussion of social breeding would be complete without reference to social insects, many of which are haplodiploid. This means that males develop from unfertilized eggs and therefore are haploid (n), having only one set of chromosomes that come from the female parent. In contrast, females, which can be either sterile workers or reproductive queens, develop from fertilized eggs and so inherit one set of chromosomes from their mother and one set from their father, which makes them diploid (2n). The relatedness between haplodiploid family members is not the same as that between diploids (Table 6.4). An important difference is that, unlike sexually reproducing diploid species, haplodiploid females are more closely related to their full-sisters (r = 0.75) than to their offspring (r = 0.5), and therefore female workers can increase their fitness by rearing sisters instead of producing their own young provided that the number of sisters is not less than two-thirds of the number of offspring that they might otherwise produce. This of course will be true only in monogynous colonies (single queen) in which the queen is inseminated by a single male, because it is only under these conditions

Table 6.4 Coefficients of relatedness in haplodiploid species. Note that a mother's relatedness to her son is 0.5 because he received only half of her genes, whereas a son's relatedness to his mother is 1.0 because all of his genes are from her. Similarly, a daughter's relatedness to her father is 0.5 because half of her genes are from him, but a father's relatedness to his daughter is 1.0 because he is haploid and therefore she has all of his genes. There is no relatedness between fathers and sons because males result from unfertilized eggs

Table 6.4 Coefficients of relatedness in haplodiploid species. Note that a mother's relatedness to her son is 0.5 because he received only half of her genes, whereas a son's relatedness to his mother is 1.0 because all of his genes are from her. Similarly, a daughter's relatedness to her father is 0.5 because half of her genes are from him, but a father's relatedness to his daughter is 1.0 because he is haploid and therefore she has all of his genes. There is no relatedness between fathers and sons because males result from unfertilized eggs

Mother

Sister

Daughter

Father

Brother

Son

Niece/nephew

Female

0.5

0.75

0.5

0.5

0.25

0.5

0.375

Male

1

0.5

1

0

0.5

0

0.25

Table 6.5 Some examples showing the average relatedness values within monogynous (one queen) and polygynous (multiple queens) colonies. In monogynous colonies a relatively high proportion of workers have at least one parent in common, and therefore overall relatedness tends to be relatively high compared with polygynous colonies

Table 6.5 Some examples showing the average relatedness values within monogynous (one queen) and polygynous (multiple queens) colonies. In monogynous colonies a relatively high proportion of workers have at least one parent in common, and therefore overall relatedness tends to be relatively high compared with polygynous colonies

Average

Type of

Species

relatedness

colony

Reference

Crab spider (Diaea ergandros)

0.44

Monogynous

Evans and Goodisman (2002)

Giant hornet (Vespa mandarinia)

0.738

Monogynous

Takahashi et al. (2004)

Carpenter ant (Camponotus

0.65

Monogynous

Goodisman and Hahn (2004)

ocreatus)

Argentine ant (Linepithema

0.007

Polygynous

Krieger and Keller (2000)

humile)

Greenhead ant (Rhytidoponera

0.082

Polygynous

Chapuisat and Crozier (2001)

metallica)

Honey bee (Apis mellifera)

0.25--0.34

Polygynous

Laidlaw and Page (1984)

that workers will be full-sisters. In colonies of the slavemaker ant (Protomognathus americanus), for example, workers are usually full-sisters with a relatedness of 0.75 and therefore will benefit by helping to raise more sisters (Foitzik and Herbers, 2001). In situations such as this, kin selection can explain why workers forego reproduction.

The situation is more complex in monogynous colonies when the queen has multiple mates, and also in polygynous colonies (multiple queens), because in these situations the relatedness of workers can range from almost 0 to around 0.75 (see Table 6.5). In polygynous colonies, worker relatedness depends not just on the number of queens but also on how closely the queens are related to one another (Ross, 2001, and references therein). Since the helpers in polygynous colonies often share few genes with the offspring, an explanation other than inclusive fitness is needed to explain this type of social breeding. Ecological factors may provide at least part of the answer, one possibility being that multiple queens are needed to ensure that enough eggs will be laid to support a colony that is large enough for long-term survival. However, this cannot explain the prevalence of helpers in colonies in which a single queen mates with multiple males, because each time a new male inseminates the queen a new set of half-siblings will be introduced into the colony and the overall within-colony relatedness will be reduced. One possible explanation in these cases is the need to increase genetic diversity within the colony.

Was this article helpful?

0 0

Post a comment