Wednesday, June 5, 2013

Supergenes, genetic determinism, and evolution

Social insects, ants, bees, termites and so forth, that are collections of individuals specialized for carrying out one of the essential tasks involved in survival of the group, are often called "superorganisms".  But even within species, different groups may exhibit different behaviors.  There is longstanding interest in whether this kind of social behavior is genetically controlled. 

An example of variable behavior is in the fire ant, Solenopsis invicta.  Some colonies have one queen while others have multiples, and that affects the organization of the rest of the colony -- indeed, colonies differ in multiple traits, including breeding strategy, how the colony reproduces, size of the queen, sex allocation, and level of aggression between colonies.  The workers in the colonies with one queen, her sterile daughters, are hostile to ants from other colonies, but the workers in colonies with multiple queens, including queens adopted from outside, coexist with those from other colonies.  But, they only tolerate queens of a specific genotype.

The genetic determinant of at least some of this behavior was identified a decade or so ago.  Kreiger and Ross (Science, 2002) found that 8 different nucleotides in the Gp-9 gene, which codes for a pheromone-binding protein, a component of the mechanism by which ants identify members of their own species, are responsible. (The specifics of this vary somewhat between colonies in North and South America but the gene and the chromosomal region are the same.)  The varying alleles, called B and b, affect development, worker behavior and queen phenotype.  A commentary on this work appeared in Trends in Genetics at the time. 
In particular, BB workers in the absence of Bb workers do not tolerate multiple queens in their colonies, so monogynous colonies are always headed by a BB queen. By contrast, Bb workers tolerate multiple queens, but only if these queens bear the b allele. Heterozygote workers somehow detect BB queens and kill them by biting, so polygynous colonies are always headed by Bb queens. Experiments suggest that Bb workers detect BB queens by sensing the lack of a surface chemical cue associated with the b allele, because workers rubbed against BB queens were killed by other workers, but those rubbed against Bb queens were not... Its bearers (Bb workers) recognize and discriminate against non-bearers (BB queens) on the basis of an external label ... Through the net outcome of these complex effects, and especially through the influence on worker behaviour, the presence or absence of the b allele among workers specifies the social structure of the colony (Table 1)
Social chromosome
A recent paper in Nature (Wang et al., "Y-like social chromosome causes alternative colony organization in fire ants") noted that Gp-9 is unlikely to control all of the behavioral differences between genotypes, and suggested that there must be other genes in the region that affect other aspects of behavior.  Wang et al. call this a 'supergene', a chromosomal region with related genes that are inherited together due to genetic linkage.  Further, they suggest it's a 'social chromosome', where polymorphisms that account for variation in social organization within species reside.  They described it thus:
The two variants, hereafter referred to as the social B and social b (SB and Sb) chromosomes, are characterized by a large region of approximately 13megabases (55% of the chromosome) in which recombination is completely suppressed between SB and Sb. Recombination seems to occur normally between the SB chromosomes but not between Sb chromosomes because Sb/Sb individuals are non-viable. Genomic comparisons revealed limited differentiation between SB and Sb, and the vast majority of the 616 genes identified in the non-recombining region are present in the two variants. The lack of recombination over more than half of the two heteromorphic social chromosomes can be explained by at least one large inversion of around 9 megabases, and this absence of recombination has led to the accumulation of deleterious mutations, including repetitive elements in the non-recombining region of Sb compared with the homologous region of SB. Importantly, most of the genes with demonstrated expression differences between individuals of the two social forms reside in the non-recombining region. These findings highlight how genomic rearrangements can maintain divergent adaptive social phenotypes involving many genes acting together by locally limiting recombination.
Fire ant colony:
So, social organization seems to be controlled by genes in a single stretch of the SB and Sb chromosomes.  These chromosomes are analogous to sex chromosomes in that the X and Y chromosomes do not recombine. Like the Y chromosome, the Sb chromosome only occurs in one of the social forms of the fire ant, so, again like the Y, it has been free to evolve genetic variation that is only expressed in one social form.  So, 70% of the genes found to be differentially expressed between the two forms are found in the non-recombining region of the chromosome. 

Supergenes of superorganisms
Now a paper in BioEssays online May 31, "Social supergenes of superorganisms: Do supergenes play important roles in social evolution?", Linksvayer et al., puts all this into a larger context.
We suggest that supergenes, groups of co-inherited loci, may be involved in a range of intriguing genetic and evolutionary phenomena in insect societies, and may play broad roles in the evolution of cooperation and conflict.  Supergenes are central in the evolution of an array of traits including self-incompatibility, mimicry, and sex chromosomes.
Linksvayer et al. suggest that similar kinds of restricted recombination scenarios will explain much of the variation in social behavior seen in social insects. They note that numerous examples of supergenes have been described, primarily in plants and fungi, but including the evolution of mimicry in butterflies, sex determination in animals and plants, genetic caste determination, and self-incompatibility in plants and fungi.

Supergenes seem often to be maintained by reduced recombination between chromosomes.  Chromosomal inversion, the reversal of a chromosome such that it cannot recombine with a copy of the chromosome that hasn't inverted, is frequently observed in supergene regions, and seems to be one way that recombination is reduced.

And, not only is recombination reduced or non-existent, as with sex chromosomes, but the genes in supergene regions seem to work so well together that that itself leads to increased fitness, again as in S invicta.  Indeed, Krieger and Ross predicted in 2002 that the Gp-9 region would include other genes that affect social behavior in fire ants.  

Supergenes and genetic determinism
We've blogged a number of times recently about the relative importance of the genetic contribution to traits.  We noted that the phenotypic similarity of inbred mice suggests that genetic determinism shouldn't be dismissed out of hand.  Indeed, the similarity between twins suggests the same.    Supergenes may be a de facto kind of inbreeding, where genetic variation is reduced at multiple genes, and thus phenotypic variation is also reduced.

If there is a restriction on recombination (and mutation), the gene segment can become essentially inbred in the population or species.  This doesn't affect the ability of mutation and recombination to generate variation elsewhere in the genomes of these populations.  Whether the restriction is due to the effects of natural selection or not is something that has to be studied on its own, but selection could be particularly effective if it doesn't have to continually sieve new recombinants of favored alleles at different genes in the complex.

In turn, this shows the potential value of a high level of genetic determinism.  If genetic effects in the target region were weak or weakly additive, then it would be unlikely that one version would outdo all the others, and one might argue that the population would be better off with the variation that recombination and mutation produce so that, as with other complex traits, changes in the environment that might favor specific trait values would find them in the population.  But most individuals  might not have viable genotypes, which might particularly occur when selection is strong.  Under these conditions, if a good combination can be fixed in the population, the selective load would be reduced.

Of course, one might expect this to yield a very vulnerable state of affairs, because if the environment changes so as not to favor the particular trait, like a social behavior pattern, the whole population could be wiped out quickly.  That's why variation is so important in evolution and why one may wonder if adaptive pressures or some mechanical factor (like chromosome inversions) rather than selection is responsible.  Whatever the truth, or truths, important issues in evolution and the function of genomes are raised by supergenes.

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