Dispatch R1083

Dispatches

Convergent Evolution: The Genetics of Queen Number in Ants Large, non-recombining genomic regions underlie the polymorphism in colony queen number in two distantly related ant species. This illustrates that convergence in complex phenotypes can arise via convergence in general genomic architecture, rather than convergent changes in specific genes. Romain Libbrecht* and Daniel J.C. Kronauer On August 16th 2014, lifeguards at Rockaway Beach in New York City mistook dolphins for sharks in the swimming area. Whistles were blown and hundreds of panicked swimmers rushed out of the water for nothing. The swimmers blamed the lifeguards for the confusion, but really they should have blamed convergent evolution: the independent origin of similar phenotypes in distinct lineages in response to similar selection pressures. While phenotypic convergence often stems from similar molecular changes when only one or a few genes are involved [1], it remains unclear to what extent convergence at the phenotypic level is associated with convergence in the underlying genetic architecture for complex, multicomponent traits. A fascinating example of such a trait can be found in ants. While ant colonies are typically headed by a single queen, several lineages have convergently evolved a more variable social organization, in which colonies can contain either one or several queens. Accepting multiple queens into the colony can be advantageous when dispersal is especially costly, for example because nest sites are patchy, habitats saturated or the environment is harsh [2]. The two types of ant societies differ not only in the number of queens, but in several other important aspects that appear to be strictly correlated (Figure 1) [3]. In this issue of Current Biology, a new study by Jessica Purcell and colleagues [4] shows that convergent evolution in ant social structure is reflected in convergence at the level of general genomic architecture, but not necessarily at the level of the actual genes involved.

The red imported fire ant Solenopsis invicta and the Alpine silver ant Formica selysi have little in common. The fire ant is globally invasive and known for its venomous sting, while the Alpine silver ant is restricted to its native range in Europe and, rather than sporting a powerful stinger, defends itself by spraying formic acid from a pore at the abdominal tip. The two also belong to separate evolutionary lineages, the ant subfamilies Myrmicinae and Formicinae, respectively. Yet, the two share an important feature: they have convergently evolved the polymorphic social organization with variation in queen number described above. In both species, queen number is associated with a whole suite of other phenotypic traits (Figure 1) [4,5]. In the early 1990s, with the advent of population genetic markers, Ken Ross from the University of Georgia discovered that social organization in fire ants was tightly correlated with the genotype at a single allozyme locus, Gp9 [6]. This locus could perfectly predict whether workers would accept or kill additional queens entering the colony and, therefore, whether colonies would end up with a single or multiple queens [7]. Although it was initially suggested that the polymorphism at the Gp9 locus, which encodes a chemosensory protein, could itself be the causal mechanism underlying the social polymorphism [8], it has since been argued that a single protein coding gene would be unlikely to regulate the many correlated phenotypic traits associated with queen number [9]. Two decades after the initial discovery of Gp9, it has now become clear that, instead of a single gene, social organization in fire ants is determined by a large non-recombining chromosomal region of more than 600 genes, which happens to contain Gp9

[5]. This social chromosome comes in two versions, termed SB and Sb (B and b being the two alleles at the Gp9 locus, and S standing for ‘‘social’’). While single queen colonies only contain SB/SB queens and workers, multiple queen colonies contain SB/Sb queens and a mix of SB/SB and SB/Sb workers. The Sb/Sb genotype is largely lethal, with very low frequencies among workers (Figure 2). To investigate the genetic basis of social organization in the Alpine silver ant, Purcell and colleagues [4] performed a genome-wide association study and constructed a genomic linkage map. This allowed them to identify a number of genetic polymorphisms that perfectly correlated with social organization, similar to what had previously been shown in fire ants. Interestingly, as in fire ants, these genetic markers all mapped to a single linkage group. The authors decided to call the two haplotypes for this social chromosome Sm (m for monogyne, i.e. single queen colonies) and Sp (p for polygyne, i.e. multiple queen colonies). Queens and workers in single queen colonies were all Sm/Sm, while queens and workers in multiple queen colonies were Sm/Sp or Sp/Sp (Figure 2). Both species have thus independently evolved a similar genomic architecture in the form of a large, non-recombining genomic region that is associated with social organization. However, there are important differences between the social chromosomes of fire ants and Alpine silver ants. First, the social chromosomes in the two species appear to contain different sets of genes. Given the incomplete assembly especially of the Alpine silver ant genome, more work will be needed to determine whether the current analysis might have missed shared genes, and/ or whether similar molecular pathways may still be involved, despite an absence of homology at the gene level. However, the finding that the overall genomic architecture — rather than the individual genes — underlying social

Current Biology Vol 24 No 22 R1084

Single queen colony

Multiple queen colony

One Number of queens Larger

More than one

Queen size

Smaller Smaller

Larger

Worker size

Higher

Queen fecundity

Lower

Lower

Nest density

Higher

Longer

Queen lifespan

Shorter

Shorter

Colony lifespan

Longer

Independent

Colony founding

Independent / Dependent Current Biology

Figure 1. Queen number in ants. In ants, colonies headed by single vs. multiple queens usually differ not only in queen number, but also in several other correlated phenotypic traits.

organization might be similar between the two species is important. Especially so, because a lot of effort is currently put into discovering genes with common functions between distantly related social insects to identify candidate genes for the evolution of sociality. Another striking difference between the two systems is that the Sb/Sb genotype is usually lethal in the fire ant, while the Sp/Sp genotype is viable in the Alpine silver ant. This not only indicates variation between the two species in the genetic determination of the social organization, but also raises the question of how similar the evolutionary history of the two social chromosomes is. The social chromosome in fire ants has been compared to sex chromosomes in that the Sb haplotype is restricted to heterozygotes and, therefore, does not recombine, just like the Y chromosome in mammals for instance. As a consequence, the Sb haplotype accumulates deleterious mutations. In contrast, because homozygotes for Sm and Sp are both viable in the Alpine silver ant, the social chromosome does not appear to accumulate significant amounts of deleterious mutations, and the comparison to sex chromosomes does not hold. This suggests that the social chromosomes in the two ant species may have very distinct evolutionary trajectories. The term ‘supergene’ has been used to refer to large genomic regions that simultaneously affect many traits and for which recombination is suppressed. Supergenes are involved in speciation and the regulation of polymorphism in many species of animals and plants

[10]. Famous examples include supergenes regulating Batesian mimicry in butterflies [11], behaviour and plumage polymorphism in birds [12] and flower morphology in plants [13]. Many of those supergenes arose from one or several chromosomal inversions that suppressed recombination. While this seems to be the case for the fire ant social chromosome, the mechanism underlying the suppression of recombination between the two variants of the Alpine silver ant social chromosome is currently unknown. Whatever the mechanism, finding a supergene regulating social

organization in two species of ant that have been evolving separately for more than 100 million years provides further evidence that supergenes may be important and common regulators of alternative phenotypes. In 1964, Bill Hamilton [14] showed that a gene promoting altruistic behaviour could be selected for in a population if its bearers preferentially directed altruistic acts towards other individuals bearing the same gene. One mechanism for this to happen, he conjectured, would be if the same gene would produce a phenotype, and lead to the recognition and preferential treatment of other individuals with that phenotype. In The Selfish Gene, Richard Dawkins [15] aptly described this mechanism with his metaphor of the ‘green beard’, according to which a green beard gene would convey the ability to produce a green beard, detect green beards, and act altruistically toward green beards. Green beard genes have long been thought of as a mostly theoretical possibility, because it seemed unlikely that a single gene could give rise to such a complex phenotype. In the fire ant, SB/Sb workers in multiple queen colonies only accept new queens that also carry the Sb haplotype. In the Alpine silver ant, the fact that no Sm/Sm queens can be found in multiple queen colonies suggests that Sm/Sp and Sp/Sp

Fire ant Solenopsis invicta Single queen colony

Alpine silver ant Formica selysi Single queen colony

Multiple queen colony

Multiple queen colony

SB/SB

SB/Sb

Queen genotype

Sm/Sm

Sm/Sp, Sp/Sp

SB/SB

SB/Sb, (Sb/Sb)

Worker genotype

Sm/Sm

Sm/Sp, Sp/Sp

SB

SB, Sb

Male genotype

Sm

Sp

12.7 megabases

Supergene size

?

616

Number of genes in supergene

?

Possibly inversion

Mechanism suppressing recombination

? Current Biology

Figure 2. Genetic basis of social organization in the fire ant and the Alpine silver ant. The genotypes at the social chromosome for ants in single queen and multiple queen colonies differ between the fire ant and the Alpine silver ant. Currently less is known about the size, content and evolution of the social chromosome in the Alpine silver ant compared to the fire ant. While fire ant colonies with multiple queens build flatter mounds than colonies with a single queen, Alpine silver ants nest in the soil under rocks, and no obvious differences in nest architecture exist between the two social forms.

Dispatch R1085

workers only accept new queens that also carry the Sp haplotype. While this remains to be investigated in the Alpine silver ant, in both species the social chromosome might dictate whether a given individual will accept another individual depending on whether it carries the same version of the social supergene or not. The social chromosomes in fire ants and Alpine silver ants demonstrate that complex green-beard phenotypes are indeed a biological reality, made possible by large green-beard supergenes. Fire ants and Alpine silver ants are by far not the only ant species with a polymorphic social organization. The finding that a similar genomic architecture underlies this polymorphism in both cases suggests the possibility that supergenes have arisen many times independently during ant evolution, and remain to be discovered in other species with flexible social organizations.

References 1. Stern, D.L. (2013). The genetic causes of convergent evolution. Nat. Rev. Genet. 14, 751–764. 2. Bourke, A.F.G., and Heinze, J. (1994). The ecology of communal breeding - the case of multiple-queen Leptothoracine ants. Phil. Trans. R. Soc. Lond. B Biol. Sci. 345, 359–372. 3. Keller, L. (1995). Social life: the paradox of multiple-queen colonies. Trends Ecol. Evol. 10, 355–360. 4. Purcell, J., Brelsford, A., Wurm, Y., Perrin, N., and Chapuisat, M. (2014). Convergent genetic architecture underlies social organization in ants. Curr. Biol. 24, 2728–2732. 5. Wang, J., Wurm, Y., Nipitwattanaphon, M., Riba-Grognuz, O., Huang, Y.-C., Shoemaker, D., and Keller, L. (2013). A Y-like social chromosome causes alternative colony organization in fire ants. Nature 493, 664–668. 6. Ross, K.G. (1992). Strong selection on a gene that influences reproductive competition in a social insect. Nature 355, 347–349. 7. Keller, L., and Ross, K.G. (1993). Phenotypic basis of reproductive success in a social insect: genetic and social determinants. Science 260, 1107–1110. 8. Keller, L., and Ross, K. (1998). Selfish genes: a green beard in the red fire ant. Nature 394, 573–575. 9. Keller, L., and Ross, K. (1999). Major gene effects on phenotype and fitness: the relative roles of Pgm-3 and Gp-9 in introduced

Self-Awareness: The Neural Signature of Disturbed Self-Monitoring A new study reveals that the illusion of feeling another person close by results from a misperception of the source and identity of sensorimotor signals of one’s own body. Gereon R. Fink Who are we? What makes us? These questions fuel fundamental debates in neuroscience. How is our self constructed? How does our mind relate us to the world surrounding us? And how do we differentiate between ourselves and others close by? In everyday life, we seem to know instantaneously and automatically how we relate to the world surrounding us; as a result, we hardly ever think about this fundamental human experience. Yet, knowing that we are the same person over time, that we are the author of our thoughts and actions, and that we are distinct from the environment are at the core of the self and self-consciousness [1]. Keeping track of the congruence between our intentions and their sensorimotor consequences is a key feature of these processes: it enables us to distinguish between events

resulting from our own actions or produced by the environment and acting upon us [2]. Normal sensorimotor states are associated with congruent motor intention and multimodal sensory experience, processes closely monitored to ensure congruency. Monitoring, in this sense, is usually implicit and automatic, but it becomes conscious whenever there is a mismatch between the expected and realized sensorimotor states. Explicit monitoring is crucial for the governance of our conscious behavior, and neurophysiological as well as functional imaging evidence implicates the prefrontal cortex as the key structure of this ‘perception–action cycle’ and active monitoring [3,4]. Converging evidence for this comes from neuropsychological data obtained from patients with frontal lobe lesions who demonstrate deficits in the planning and regulation of their

10.

11.

12.

13. 14. 15.

populations of the fire ant Solenopsis invicta. J. Evol. Biol. 12, 672–680. Schwander, T., Libbrecht, R., and Keller, L. (2014). Supergenes and complex phenotypes. Curr. Biol. 24, R288–R294. Joron, M., Papa, R., Beltra´n, M., Chamberlain, N., Mava´rez, J., Baxter, S., Abanto, M., Bermingham, E., Humphray, S.J., and Rogers, J. (2006). A conserved supergene locus controls colour pattern diversity in Heliconius butterflies. PLoS Biol. 4, e303. Thomas, J.W., Ca´ceres, M., Lowman, J.J., Morehouse, C.B., Short, M.E., Baldwin, E.L., Maney, D.L., and Martin, C.L. (2008). The chromosomal polymorphism linked to variation in social behavior in the white-throated sparrow (Zonotrichia albicollis) is a complex rearrangement and suppressor of recombination. Genetics 179, 1455–1468. Gilmartin, P., and Li, J. (2010). Homing in on heterostyly. Heredity 105, 161–162. Hamilton, W.D. (1964). The genetical evolution of social behaviour. II. J. Theoret. Biol. 7, 17–52. Dawkins, R. (1976). The Selfish Gene (Oxford: Oxford University Press).

Laboratory of Insect Social Evolution, The Rockefeller University, 1230 York Avenue, New York, NY 10065, USA. *E-mail: [email protected] http://dx.doi.org/10.1016/j.cub.2014.09.066

behavior [5,6]. Based on such experimental and clinical data, as well as computer simulations, cognitive scientists build models of how the mind works. Such models can then be tested by relating mental faculties to distinct brain areas using neuroimaging or electrophysiology combined with lesion symptom inferences. From such reasoning, disordered self-monitoring has long been associated with one class of symptoms often observed in patients suffering from schizophrenia: it has been suggested that symptoms such as auditory hallucinations and delusion of control may result from a failure in the mechanisms by which the predicted consequences of a self-produced action are derived from an internal forward model [7]. Consistent with this suggestion, hallucinating schizophrenics show deficits in tasks that require self-monitoring [8]. A paper in this issue of Current Biology [9] now reports important findings suggesting that the strange sensation that somebody is nearby (and typically behind) when no one is actually present and hence cannot be seen — the ‘feeling of presence’ — is caused by misperceiving the source and identity of sensorimotor signals of one’s own body.

Convergent evolution: the genetics of queen number in ants.

Large, non-recombining genomic regions underlie the polymorphism in colony queen number in two distantly related ant species. This illustrates that co...
215KB Sizes 0 Downloads 7 Views