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An indirect test of inbreeding depression in the termites Reticulitermes flavipes and Reticulitermes virginicus

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Abstract

We analyzed tandem-running pairs of the termites Reticulitermes flavipes and Reticulitermes virginicus utilizing 13 and 12 microsatellite loci, respectively. Newly formed pairs in both species were significantly related to one another, but this average relatedness was considerably higher in R. flavipes (0.130 vs 0.060). These average relatedness levels resulted from some tandem pairs forming between nestmate termites: more than one quarter of all R. flavipes pairs (26.1%) met this criterion, while this was the case for only about one of every 20 R. virginicus pairs (5.1%). The likelihood that termites paired with siblings was inversely related to the inferred dispersal ability of the two species. F ST, measured over identical spatial scales, was significantly higher in R. flavipes (0.034) than in R. virginicus (0.008). A comparison in R. flavipes of the observed proportion of nestmate pairs observed during tandem running vs the proportion found in established colonies revealed a significant excess of close relatives when pairs were first formed. There are two possible causes of this discrepancy: inbreeding depression (ID) may eliminate inbred colonies early in development, or related pairs may part late in the tandem-running phase or after it is completed. The latter explanation of inbreeding avoidance implies either historical or contemporary ID, and these results therefore suggest that, either directly or indirectly, ID could be a more potent force in the evolution of termite mating systems than is generally appreciated.

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References

  • Avilés L (1997) Causes and consequences of cooperation and permanent-sociality in spiders. In: Crespi BJ, Choe J (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge UK, pp 476–498

    Google Scholar 

  • Barrett SCH (1998) The evolution of mating strategies in flowering plants. Trends Plant Sci 3:335–341

    Article  Google Scholar 

  • Barrett SCH, Harder LD (1996) Ecology and evolution of plant mating. Trends Ecol Evol 11:73–79

    Article  Google Scholar 

  • Bartz SH (1979) Evolution of eusociality in termites. Proc Natl Acad Sci U S A 76:5764–5768 (correction, PNAS 77:3070)

    Article  PubMed  CAS  Google Scholar 

  • Bilde T, Lubin Y, Smith DR, Schneider JM, Maklakov AA (2005) The transition to social inbred mating systems in spiders: role of inbreeding tolerance in a subsocial predecessor. Evolution 59:160–174

    PubMed  Google Scholar 

  • Bossart JL, Prowell DP (1998) Genetic estimates of population structure and gene flow: limitations, lessons and new directions. Trends Ecol Evol 13:202–206

    Article  Google Scholar 

  • Braude S (2000) Dispersal and new colony foundation in wild naked mole-rats: evidece against inbreeding as the system of mating. Behav Ecol 11:7–12

    Article  Google Scholar 

  • Bulmer MS, Adams ES, Traniello JFA (2001) Variation in colony structure in the subterranean termite Reticulitermes flavipes. Behav Ecol Sociobiol 49:236–243

    Article  Google Scholar 

  • Byers DL, Waller DM (1999) Do plant populations purge their genetic load? Effects of population size and mating history on inbreeding depression. Annu Rev Ecol Syst 30:479–513

    Article  Google Scholar 

  • Chapuisat M (1998) Mating frequency of ant queens with alternative dispersal strategies, as revealed by microsatellite analysis of sperm. Mol Ecol 7:1097–1105

    Article  Google Scholar 

  • Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst 18:237–268

    Article  Google Scholar 

  • Ciszek D (2000) New colony formation in the "highly inbred" eusocial naked mole-rat: outbreeding is preferred. Behav Ecol 11:1–6

    Article  Google Scholar 

  • Cook JM, Crozier RH (1995) Sex determination and population biology in the Hymenoptera. Trends Ecol Evol 10:281–286

    Article  Google Scholar 

  • DeHeer CJ, Vargo EL (2004) Colony genetic organization and colony fusion in the termite Reticulitermes flavipes as revealed by foraging patterns over time and space. Mol Ecol 13:431–441

    Article  PubMed  Google Scholar 

  • DeHeer CJ, Kutnik M, Bagnères A-G, Vargo EL (2005) The breeding system and population structure of the termite Reticulitermes grassei in southwestern France. Heredity 95:408–415

    Article  PubMed  CAS  Google Scholar 

  • Dronnet S, Bagnères A-G, Juba TR, Vargo EL (2004) Polymorphic microsatellite loci in the European subterranean termite, Reticulitermes santonensis Feytaud. Mol Ecol Notes 4:127–129

    Article  CAS  Google Scholar 

  • Dronnet S, Chapuisat M, Vargo EL, Lohou C, Bagnères A-G (2005) Genetic analysis of the breeding system of an invasive subterranean termite, Reticulitermes santonensis, in urban and natural habitats. Mol Ecol 14:1311–1320

    Article  PubMed  CAS  Google Scholar 

  • Fei HX, Henderson G (2003) Comparative study of incipient colony development in the Formosan subterranean termite Coptotermes formosanus Shiraki (Isoptera, Rhinotermitidae). Insect Soc 50:201–297

    Article  Google Scholar 

  • Hamilton WD (1972) Altruism and related phenomena, mainly in social insects. Annu Rev Ecol Syst 3:193–232

    Article  Google Scholar 

  • Hedrick PW (1999) Perspective: highly variable loci and their interpretation in evolution and conservation. Evolution 53:313–318

    Article  Google Scholar 

  • Hedrick PW, Kalinowski ST (2000) Inbreeding depression in conservation biology. Annu Rev Ecol Syst 31:139–162

    Article  Google Scholar 

  • Henter HJ (2003) Inbreeding depression and haplodiploidy: experimental measures in a parasitoid and comparisons across diploid and haplodiploid insect taxa. Evolution 57:1793–1803

    PubMed  Google Scholar 

  • Howard RW, Jones SC, Mauldin JK, Beal RH (1982) Abundance, distribution, and colony size estimates for Reticulitermes spp (Isoptera: Rhinotermitidae) in southern Mississippi. Environ Entomol 11:1290–1293

    Google Scholar 

  • Husband BC, Schemske DW (1996) Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50:54–70

    Article  Google Scholar 

  • Husseneder C, Messenger MT, Su N-Y, Grace JK, Vargo EL (2005) Colony social organization and population genetic structure of an introduced population of the Formosan Subterranean Termite from New Orleans, Louisiana, USA. J Econ Entomol (in press)

  • Jarvis JUM, O’Riain MJ, Bennett NC, Sherman PW (1994) Mammalian eusociality: a family affair. Trends Ecol Evol 9:47–51

    Article  Google Scholar 

  • Jones SC, La Fage JP, Howard RW (1988) Isopteran sex ratios: phylogenetic trends. Sociobiology 14:89–156

    Google Scholar 

  • Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241

    Article  Google Scholar 

  • Michod RE (1980) Evolution of interactions in family-structured populations: mixed mating models. Genetics 96:275–296

    PubMed  CAS  Google Scholar 

  • Myles TG (1999) Review of secondary reproduction in termites (Insecta: Isoptera) with comments on its role in termite ecology and social evolution. Sociobiology 33:1–87

    Google Scholar 

  • Nutting WL (1969) Flight and colony foundation. In: Krishna K, Weesner FM (eds) Biology of termites, vol 1. Academic, New York, pp 233–282

    Google Scholar 

  • Pearce MJ (1997) Termites: biology and pest management. CAB International, New York, NY

    Google Scholar 

  • Pusey A, Wolf M (1996) Inbreeding avoidance in animals. Trends Ecol Evol 11:201–206

    Article  Google Scholar 

  • Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275

    Article  Google Scholar 

  • Reilly LM (1987) Measurements of inbreeding and average relatedness in a termite population. Am Nat 130:339–349

    Article  Google Scholar 

  • Rosengaus RB, Traniello JFA (1993) Disease risk as a cost of outbreeding in the termite Zootermopsis angusticollis. Proc Natl Acad Sci U S A 90:6641–6645

    Article  PubMed  CAS  Google Scholar 

  • Ross KG (2001) Molecular ecology of social behaviour: analyses of breeding systems and genetic structure. Mol Ecol 10:265–284

    Article  PubMed  CAS  Google Scholar 

  • Rüppell O, Heinze J, Hölldobler B (2002) Intracolonial patterns of reproduction in the queen-size dimorphic ant Leptothorax rugatulus. Behav Ecol 13:239–247

    Article  Google Scholar 

  • Shellman-Reeve JS (1996) Operational sex ratios and lipid reserves in the dampwood termite Zootermopsis nevadensis (Hagen) (Isoptera: Termopsidae). J Kans Entomol Soc 69:139–146

    Google Scholar 

  • Shellman-Reeve JS (2001) Genetic relatedness and partner preference in a monogamous, wood-dwelling termite. Anim Behav 61:869–876

    Article  Google Scholar 

  • Snyder TE (1935) Our enemy the termite. Comstock, Ithaca, NY

    Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry. Freeman, New York NY

    Google Scholar 

  • Sundström L, Keller L, Chapuisat M (2003) Inbreeding and sex-biased gene flow in the ant Formica exsecta. Evolution 57:1552–1561

    PubMed  Google Scholar 

  • Thompson GJ, Hebert PDN (1998) Population genetic structure of the Neotropical termite Nasutitermes nigriceps (Isoptera: Termitidae). Heredity 80:48–55

    Article  Google Scholar 

  • Thorne BL, Traniello JFA, Adams ES, Bulmer MS (1999) Reproductive dynamics and colony structure of subterranean termites of the genus Reticulitermes (Isoptera Rhinotermitidae): a review of the evidence from behavioral, ecological, and genetic studies. Ethol Ecol Evol 11:149–169

    Article  Google Scholar 

  • Uyenoyama MK (1984) Inbreeding and the evolution of altruism under kin selection: effects of relatedness and group structure. Evolution 38:778–795

    Article  Google Scholar 

  • Vargo EL (2000) Polymorphism at trinucleotide microsatellite loci in the subterranean termite Reticulitermes flavipes. Mol Ecol 9:817–829

    Article  PubMed  CAS  Google Scholar 

  • Vargo EL (2003a) Genetic structure of Reticulitermes flavipes and R. virginicus (Isoptera: Rhinotermitidae) colonies in an urban habitat and tracking of colonies following treatment with hexaflumuron bait. Environ Entomol 32:1271–1282

    Article  Google Scholar 

  • Vargo EL (2003b) Hierarchical analysis of colony and population genetic structure in the eastern subterranean termite, Reticulitermes flavipes, using two classes of molecular markers. Evolution 57:2805–2818

    PubMed  CAS  Google Scholar 

  • Wang S, Hard JJ, Utter F (2002) Salmonid inbreeding: a review. Rev Fish Biol Fish 11:301–319

    Article  Google Scholar 

  • Waser PM, Austad SM, Keane B (1986) When should animals tolerate inbreeding? Am Nat 128:529–537

    Article  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

Download references

Acknowledgements

Tom Juba provided assistance in the field and in the laboratory. To the best of our knowledge, we performed this work in accordance with state and federal laws regulating scientific research.

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Correspondence to Christopher J. DeHeer.

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Communicated by J. Heinze

This work was funded by grants from the United States Department of Agriculture National Research Initiative Competitive Grants Program (nos. 00-35302-9377 and 2002-35302-12490).

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DeHeer, C.J., Vargo, E.L. An indirect test of inbreeding depression in the termites Reticulitermes flavipes and Reticulitermes virginicus . Behav Ecol Sociobiol 59, 753–761 (2006). https://doi.org/10.1007/s00265-005-0105-9

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  • DOI: https://doi.org/10.1007/s00265-005-0105-9

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