Jon Hess
Campus Box 1137
Department of Biology
Washington University
St. Louis, MO 63130
(314) 935-6867
jehess@artsci.wustl.edu
The Role of Mating Structure in Eusociality: Challenging the Notion of an "Inbreeding" Naked Mole Rat (Heterocephalus glaber)
Studies reporting low levels of genetic variation for the naked mole rat (Heterocephalus glaber) were biased because they sampled a bottleneck (1,2,3, for explantation see 4). These studies concluded that the mole rats were inbreeding resulting in siblings sharing high levels of genetic variation. Inclusive fitness could then be invoked to explain the maintenance of their eusocial behavior, which is a colony structure with a pair of breeders and their nonbreeding worker progeny. H. glaber individuals were also thought to be unable to survive in the absence of a huge colony so it was proposed that new colonies formed by a fissioning of existing colonies (5). All these factors were combined to support the hypothesis that naked mole rats had adopted a mating structure of isolated groups of closely related individuals that were involved in consanguineous matings resulting in a stable unit of kin cooperation. This hypothesis has been widely popular because of its genetic basis and apparent similarity to Hamilton’s explanation for eusociality in the hymenopteran insects (6,7,8,9). However, the hypothesis has ignored the ecological factors that must also play a role in the maintenance of eusocial behavior (2,9). Recent
demographic studies and laboratory experiments reporting frequent dispersion and outbreeding preference have raised doubts about the inbreeding hypothesis (4,10,11). I would like to elucidate the mating structure of H. glaber to test hypotheses concerning the mechanisms that have generated low variation within and between the eusocial colonies. I plan on testing the following null hypotheses: 1) the system of mating is random mating, and 2) there is no gene flow between colonies.
Microsatellites are ideal for testing these hypotheses because their variability allow studies at different scales (12). I will make species-specific primers for H. glaber using a microsatellite enriching protocol (13). I have access to the DNA of over 7000 naked mole rat individuals that were collected over 14 years from 54 colonies in a 6-km2 area in Meru National Park, Kenya, along with mark-recapture and ecological data for the same individuals. I am also planning to complete a grid-like sampling of the entire 870 km2 park. Comparing observed allele frequencies with those expected under random mating, I will test the system of mating (14). Gene flow will be estimated using allele frequency differences between populations and the partitioning of genetic variation among colonies (15). These parameters are commonly estimated using data from microsatellites in species ranging from komodo dragons to mice and beluga whales (16,17,18).
References

1 Faulkes, C. G., D. H. Abbott, et al. (1990). "Investigation of genetic diversity in wild colonies of naked mole-rats (Heterocephalus glaber) by DNA fingerprinting. Journal of Zoology 221:87-97.
2 Reeve, H. K., D. F. Westneat, et al. (1990). "DNA Fingerprinting Reveals High-Levels of Inbreeding in Colonies of the Eusocial Naked Mole-Rat." Proceedings of the National Academy of Sciences of the United States of America 87(7): 2496-2500.
3 Honeycutt, R. L., K. Nelson, et al. (1991). "Genetic variation with and among populations of the naked mole-rat: evidence from nuclear and mitochondrial genomes." In: The biology of the naked mole-rat (Sherman PW, Jarvis JUM, Alexander RD, eds). Princeton, New Jersey: Princeton University Press; 195-208.
4 Braude, S. (2000). "Dispersal and new colony formation in wild naked mole-rats: evidence against inbreeding as the system of mating." Behavioral Ecology 11(1): 7-12.
5 Brett, R. A. (1991). "The population structure of naked mole-rat colonies." In: The biology of the naked mole-rat (Sherman PW, Jarvis JUM, Alexander RD, eds). Princeton, New Jersey: Princeton University Press; 97-136.
6 Sherman, P. W., J. U. M. Jarvis, et al. (1992). "Naked mole-rats." Scientific American 267:72-78.
7 Honeycutt, R. L. (1992). "Naked mole-rats." American Science 80:43-53.
8 Freeman, S., J. C. Herron. (1998). Evolutionary analysis. Upper Saddle River, New Jersey: Princeton Hall.
9 Hamilton, W. D. (1964). The genetic evolution of social behavior. Journal of Theoretical Biology 7:1-52.
10 Ciszek, D. (2000). "New colony formation in the "highly inbred" eusocial naked mole-rat: outbreeding is preferred." Behavioral Ecology 11(1): 1-6.
11 Clarke, F. M. and C. G. Faulkes (1999). "Kin discrimination and female mate choice in the naked mole-rat Heterocephalus glaber." Proceedings of the Royal Society of London Series B-Biological Sciences 266(1432): 1995-2002.
12 Goldstein, D. B. and C. Schlotterer, Eds. (1999). Microsatellites: Evolution and Applications. New York, Oxford University Press.
13 Hamilton, M. B., E. L. Pincus, et al. (1999). "Universal linker and ligation procedures for construction of genomic DNA libraries enriched for microsatellites." Biotechniques 27(3): 500-+.
14 Templeton, A. R. and B. Read (1994). Inbreeding: one word, several meanings, much confusion. Conservation Genetics. V. Loeschcke, J. Tomiuk and S. K. Jain. Switzerland, Birkhauser Verlag Basel: 91-105.
15 Slatkin, M. (1995). "A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457-462.
16 Ciofi, C. and M. W. Bruford (1999). "Genetic structure and gene flow among Komodo dragon populations inferred by microsatellite loci analysis." Molecular Ecology 8(12): S17-S30.
17 Dallas, J. F., B. Dod, et al. (1995). "Population Subdivision and Gene Flow in Danish House Mice." Molecular Ecology 4(3): 311-320.
18 Gladden, J. G. B., M. M. Ferguson, et al. (1999). "Population structure of North American beluga whales (Delphinapterus leucas) based on nuclear DNA microsatellite variation and contrasted with the population structure revealed by mitochondrial DNA variation." Molecular Ecology 8(3): 347-363.
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