Abstract
Understanding levels of population differentiation and inbreeding are important issues in conservation biology, especially for social Hymenoptera with fragmented and small population sizes. Isolated populations are more vulnerable to genetic loss and extinction than those with extended continuous distributions. However, small populations are not always a consequence of a recent reduction of their habitat. Thus, determining the history of population isolation and current patterns of genetic variation of a species is crucial for its conservation. Rossomyrmex minuchae is a slave-making ant with patchy distribution in South Eastern Spain and is classified as vulnerable by the IUCN. In contrast, the other three known species of the genus are presumed to show more uniform distributions. Here we investigate the genetic diversity and population structure of R. minuchae and compare it with that found in two other species of the genus: R. anatolicus and R. quandratinodum. We conclude that although genetic diversity of R. minuchae is low, there is no evidence of a recent bottleneck, suggesting a gradual and natural fragmentation process. We also show extreme population differentiation at nuclear and mitochondrial markers, and isolation by distance at a local scale. Despite some evidence for inbreeding and low genetic variation within populations, we found almost no diploid males, a finding which contrasts with that expected in inbred Hymenoptera with single locus complementary sex determination. This could mean that sex is determined by another mechanism. We argue that continued low population size means that detrimental effects of inbreeding and low genetic variation are likely in the future. We suggest that a policy of artificial gene flow aimed at increasing within population variation is considered as a management option.
Similar content being viewed by others
References
Beukeboom L (1995) Sex determination in Hymenoptera—a need for genetic and molecular studies. Bioessays 17:813–817
Boomsma JJ, Ratnieks FLW (1996) Paternity in eusocial Hymenoptera. Phil Trans R Soc B 351:947–975
Brandt M, Fischer-Blass B, Heinze J, Foitzik S (2007) Population structure and the co-evolution between social parasites and their hosts. Mol Ecol 16:2063–2078
Brunner E, Trindl A, Falk KH, Heinze J, D’Ettorre P (2005) Reproductive conflict in social insects: male production by workers in a slave-making ant. Evolution 59:2480–2482
Buschinger A (1989) Evolution, speciation, and inbreeding in the parasitic ant genus Epimyrma (Hymenoptera, Formicidae). J Evol Biol 2:265–283
Chapman RE, Bourke AFG (2001) The influence of sociality on the conservation biology of social insects. Ecol Lett 4:650–662
Chapuisat M (1996) Characterization of microsatellite loci in Formica lugubris and their variability in other ant species. Mol Ecol 5:560–599
Clémencet J, Viginier B, Doums C (2005) Hierarchical analysis of population genetic structure in the monogynous ant Cataglyphis cursor using microsatellite and mitochondrial DNA markers. Mol Ecol 14:3735–3744
Cook JM, Crozier RH (1995) Sex determination and population biology in the Hymenoptera. TREE 10:281–286
Crozier RH (1971) Heterozygosity and sex determination in haplodiploidy. Am Nat 105:399–412
Darvill B, Ellis JS, Lye GC, Goulson D (2006) Population structure and inbreeding in a rare and declining bumblebee, Bombus muscorum (Hymenoptera: Apidae). Mol Ecol 15:601–611
Fischer-Blass B, Heinze J, Foitzik S (2006) Microsatellite analysis reveals strong but differential impact of a social parasite on its two host species. Mol Ecol 15:863–872
Foster KR, Ratnieks FLW, Raybould AF (2000) Do hornets have zombie workers? Mol Ecol 9:735–742
Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge, UK
Goropashnaya AV, Seppä P, Pamilo P (2001) Social and genetic characteristics of geographically isolated populations in the ant Formica cinerea. Mol Ecol 10:2807–2818
Goudet J (2002) FSTAT A program to estimate and test gene diversities and fixation indices (Version 2932) Available from www.unilch/izea/softwares/fstathtml
Gyllenstrand N, Gertsch PJ, Pamilo P (2002) Polymophic microsatellite DNA markers in the ant Formica exsecta. Mol Ecol Notes 2:67–69
Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol 13:3621–3632
Hardy OJ, Pearcy M, Aron S (2008) Small-scale spatial genetic structure in an ant species with sex-biased dispersal. Biol J Linn Soc 93:465–473
Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638
Heinze J, Hölldobler B, Yamuchi K (1998) Male competition in Cardiocondyla ants. Behav Ecol Sociobiol 42:239–246
Keller LF, Waller DM (2002) Inbreeding effects in wild populations. TREE 17:230–241
Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary analysis and sequence alignment. Brief Bioinform 5:150–163
Loftis DG, Echelle AA, Koike H, Van Den Bussche RA, Minckley CO (2009) Genetic structure of wild populations of the endangered Desert Pupfish complex (Cyprinodontidae: Cyprinodon). Conserv Genet 10:453–463
Luikart G, Allendorf FW, Cornuet JM, Sherwin WB (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–247
Mäki-Petäys H, Breen J (2007) Genetic vulnerability of a remnant ant population. Conserv Genet 8:427–435
Mäki-Petäys H, Zakharov A, Viljakainen L, Corander J, Pamilo P (2005) Genetic changes associated to declining populations of Formica ants in fragmented forest landscape. Mol Ecol 14:733–742
Mantel M (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220
Marikovsky PY (1974) The biology of the ant Rossomyrmex proformicarum K. W. Arnoldi (1928). Insect Soc 21:301–308
Martínez-Ibáñez MD, Tinaut A, Ruano F (2006) Rossomyrmex minuchae Tinaut 1981. In: Verdú JR, Galante E (eds) Libro Rojo de los Invertebrados de España. Dirección General para la Biodiversidad Ministerio de Medio. Ambiente, Madrid, pp 1167–1170
Meirmans PG (2006) Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution 60:2399–2402
Mockford SW, Herman TB, Snyder M, Wright JM (2007) Conservation genetics of Blanding’s turtle and its application in the identification of evolutionarily significant units. Conserv Genet 8:209–219
Moilanen A, Sundström L, Pedersen JS (2004) MateSoft: a program for deducing parental genotypes and estimating mating system statistics in haplodiploid species. Mol Ecol Notes 4:795–797
Moritz C (1994) Defining evolutionarily-significant-units for conservation. TREE 9:373–375
New TR (1995) An introduction to invertebrate conservation biology. Oxford University Press, Oxford
Pabijan M, Babik W, Rafinski J (2005) Conservation units in north-eastern populations of the Alpine newt (Triturus alpestris). Conserv Genet 6:307–312
Pamilo P (1993) Polyandry and allele frequency differences between sexes in the ant Formica aquilonia. Heredity 70:472–480
Pamilo P, Crozier RH (1997) Population biology of social insect conservation. Mem Mus Vic 56:411–419
Pearcy M, Clemencet J, Chameron S, Aron S, Doums C (2004) Characterization of nuclear DNA microsatellite markers in the ant Cataglyphis cursor. Mol Ecol Notes 4:642–644
Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275
Raymond M, Rousset F (1995) GENEPOP: population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Ross KG, Keller L (1995) Ecology and evolution of social organization: insights from fire ants and other highly eusocial insects. Annu Rev Ecol Syst 26:631–656
Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228
Ruano F, Tinaut A (1999) Raid process activity pattern and influence of abiotic conditions in Rossomyrmex minuchae (Hymenoptera: Formicidae) a slave-maker species. Insect Soc 46:341–347
Ruano F, Tinaut A (2005) Mating behaviour in a slave-making ant Rossomyrmex minuchae (Hymenoptera Formicidae). Naturwissenschaften 92:328–331
Ruano F, Tinaut A, Sanllorente O, Fernández-Zambrano A (2007) Nuevas localidades para Rossomyrmex minuchae (Hymenoptera Formicidae). Bol Asoc esp Ent 31:209–211
Samways MJ (1994) Insect conservation biology. Chapman & Hall, London
Samways MJ (2005) Insect diversity conservation. Cambridge University Press, Cambridge
Schrempf A, Reber C, Tinaut A, Heinze J (2005) Inbreeding and local mate competition in the ant Cardiocondyla batesii. Behav Ecol Sociobiol 57:502–510
Schrempf A, Aron S, Heinze J (2006) Sex determination and inbreeding depression in an ant with regular sib-mating. Heredity 97:75–80
Sundström L, Keller L, Chapuisat M (2003) Inbreeding and sex-biased gene flow in the ant Formica exsecta. Evolution 57:1552–1561
Sundström L, Seppä P, Pamilo P (2005) Genetic population structure and dispersal patterns in Formica ants—a review. Ann Zool Fennici 42:163–177
Thomas JA (1994) Why small cold-blooded insects pose different conservation problems to birds in modern landscapes. Ibis 137:S112–S119
Tinaut A, Ruano F, Sanllorente O, Fernández-Zambrano A, Karaman C and Kaz Y (2010) Nest composition and worker relatedness in three slave making ants of the genus Rossomyrmex Arnoldi and their Proformica Ruzsky hosts (Hymenoptera, Formicidae). Insect Sci 17
Trontti K, Aron S, Sundström L (2006) The genetic population structure of the ant Plagiolepis xene-implications for genetic vulnerability of obligate social parasites. Conserv Genet 7:241–250
van Wilgenburg E, Driessen G, Beukeboom LW (2006) Single locus complementary sex determination in Hymenoptera: an “unintelligent” design? Front Zool 3:1
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Wilson EO (1971) The insect societies. Belknap Press, Cambridge, MA
Woyke J (1963) What happens to diploid drone larvae in a honeybee colony. J Apic Res 2:73–75
Zayed A, Packer L (2005) Complementary sex determination substantially increases extinction proneness of haplodiploid populations. Proc Natl Acad Sci USA 102:10742–10746
Acknowledgements
We thank the directorate of the National Park of Sierra Nevada for allowing us to sample there. A. Fernández, C. Karaman and Y. Kaz for helping us in nest search and excavations in Spain, Turkey and Kazakhstan, respectively. F. Mier and Y. Kaz kindly helped us with bureaucracy in Kazakhstan. J.G. Martínez offered technical help and J.D. Ibáñez-Álamo created the map. We also thank two anonymous reviewers for very useful comments. This research was supported by Ministerio de Medio Ambiente, Organismo Autónomo Parques Nacionales, project ref: 78/2003, a FPU grant to O.S. (Ministerio de Educación), the Plan Propio of the University of Granada and the Swiss NSF.
Author information
Authors and Affiliations
Corresponding author
Additional information
O. Sanllorente and R. L. Hammond are joint first authors.
Rights and permissions
About this article
Cite this article
Sanllorente, O., Hammond, R.L., Ruano, F. et al. Extreme population differentiation in a vulnerable slavemaking ant with a fragmented distribution. Conserv Genet 11, 1701–1710 (2010). https://doi.org/10.1007/s10592-010-0063-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-010-0063-2