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Simple method for combining multiple-loci marker genotypes to estimate diploid male proportion, with an application to a threatened bumble bee population in Japan

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Abstract

Production of diploid males is disadvantageous for populations of haplodiploid species, because it increases the genetic load and decreases fitness. In social species, the damage becomes more serious because of increased colony mortality and decreased colony growth rates. As a parameter to quantify diploid male production, the proportion of diploids that are males, \(\Phi\), has been estimated using multiple-loci marker genotypes. In these studies, \(\Phi\) is separately estimated for individual marker locus, and then the estimates are averaged over marker loci. In this paper, we propose a simple method for combining genotypes of multiple-marker loci to obtain a single estimate of \(\Phi\), which is expected to enhance the quality of estimate. As an application, \(\Phi\) in a threatened bumble bee population in Japan is estimated from genotype data of multiple microsatellite loci. Under the separate analysis of individual marker locus the detectability of diploid males, measured by the probability that a diploid is heterozygous, is within the range of 0.196–0.554, whereas the detectability from the proposed method increases to 0.834, giving an estimate of \(\Phi\) with a higher degree of precision.

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References

  • Adams J, Rothman ED, Kerr WE, Paulino ZL (1977) Estimation of the number of sex alleles and queen matings from diploid male frequencies in a population of Apis mellifera. Genetics 86:583–596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carvalho GA (2001) The number of sex alleles (CSD) in a bee population and its practical importance (Hymenoptera: Apidae). J Hym Res 10:10–15

    Google Scholar 

  • Cook JM (1993) Sex determination in the Hymenoptera: a review of models and evidence. Heredity 71:421–435

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Cornuet JM (1980) Rapid estimation of the number of sex alleles in panmictic honeybee populations. J Apic Res 19:3–5

    Article  Google Scholar 

  • Crozier RH, Pamilo P (2003) Evolution of social insect colonies. Sex allocation and kin selection. Oxford University Press, Oxford

    Google Scholar 

  • Darvill B, Knight ME, Lye GC, Goulson D (2006) Population structure and inbreeding in a rare and declining bumblebee, Bombus muscorum (Hymenoptera: Apidae). Mol Ecol 15:601–611

    Article  CAS  PubMed  Google Scholar 

  • Duchateau MJ, Hoshida H, Velthuis HHW (1994) Diploid males in the bumblebee Bombus terrestris: sex determination, sex alleles and viability. Entomol Exp Appl 71:263–269

    Article  Google Scholar 

  • Ellis JS, Knight ME, Darvill B, Goulson D (2006) Extremely low effective population sizes, genetic structuring and reduced genetic diversity in a threated bumblebee species, Bombus sylvarum (Hymenoptera: Apidae). Mol Ecol 15:4375–4386

    Article  CAS  PubMed  Google Scholar 

  • Faria LRR, Soares FDG, do Carmo E, de Oliveria PMC (2016) Diploid male dynamics under different numbers of sex alleles and male dispersal abilities. Theory Biosci 135:111–119

    Article  PubMed  Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Giangarelli DC, Freiria GA, Ferreira DG, Aguiar WM, Penha RES, Alves AN, Gaglianone MC, Sofia SH (2015) Orchid bees: a new assessment in the rarity of diploid males in populations of this group of Neotropical pollinators. Apidologie 46:606–617

    Article  Google Scholar 

  • Goulson D (2010) Bumblebees, behaviour, ecology and conservation, 2nd edn. Oxford University Press, Oxford

    Google Scholar 

  • Harpur BA, Sobhani M, Zayed A (2012) A review of the consequences of complementary sex determination and diploid male production on mating failures in the Hymenoptera. Entomol Exp Appl 146:156–164

    Article  Google Scholar 

  • Hein S, Poethke H-J, Dorn S (2009) What stop the ‘diploid male vortex’? A simulation study for species with single locus complementary sex determination. Ecol Model 220:1963–1669

    Article  Google Scholar 

  • Kerr WE (1987) Sex determination in bees. XXI. Number of XO-heteroalleles in a natural population of Melipona compressipes fasciculata (Apidae). Insect Soc 34:274–279

    Article  Google Scholar 

  • Kukuk PF, May B (1990) Diploid males in primitively eusocial bee, Lasioglossum (Dialictus) zephyyrum (Hymenoptera: Halictidae). Evolution 44:1522–1528

    PubMed  Google Scholar 

  • Nomura T, Sasaki T, Taniguchi Y (2021) A molecular genetic method for estimating nest density in bumblebee populations without explicit definition of habitat area. J Insect Conserv 25:695–706

    Article  Google Scholar 

  • Owen RE, Packer L (1994) Estimation of the production of diploid males in populations of Hymenoptera. Heredity 72:219–227

    Article  Google Scholar 

  • Page RE (1980) The evolution of multiple mating behavior by honey bee queens (Apis mellifera). Genetics 96:263–273

    Article  PubMed  PubMed Central  Google Scholar 

  • Plowight RC, Palett MJ (1979) Worker-male conflict and inbreeding in bumble bees (Hymenoptera; Apidae). Can Entomol 111:289–294

    Article  Google Scholar 

  • Ross KG, Fletcher DJC (1986) Diploid male production—a significant colony mortality factor in the fire ant Solenopsis invicta (Hymenoptera: Formicidae). Behav Ecol Sociobiol 19:283–291

    Article  Google Scholar 

  • Ross KG, Vargo EL, Keller L, Trager JC (1993) Effect of a founder even on variation in the genetic sex-determining system of the fire ant Solenopsis invivta. Genetics 135:843–854

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shao ZY, Mao HX, Fu WJ (2004) Genetic structure of Asian populations of Bombus ignites (Hymenoptera: Apidae). J Hered 95:46–52

    Article  CAS  PubMed  Google Scholar 

  • Souza RO, Del Lama MA, Cervini M et al (2010) Conservation genetics of neotropical pollinators revised: microsatellite analysis suggests that diploid males are rare in orchid bees. Evolution 64:3318–3326

    Article  PubMed  Google Scholar 

  • Takahashi J, Ayabe T, Mitsuhata M, Shimizu I, Ono M (2008) Diploid male production in a rare and locally distributed bumblebee, Bombus florilegus (Hymenoptera: Apidae). Insct Soc 55:43–50

    Article  Google Scholar 

  • Takahashi J, Sasaki T, Nishimoto M, Okuyama H, Nomura T (2018) Characterization of the complete sequence analysis of mitochondrial DNA of Japanese rare bumblebee species, Bombus Cryptarum florilegus. Conserv Genet Resour 10:387–391

    Article  Google Scholar 

  • Takeuchi T, Sasaki T, Mitsuhata M, Kiyoshi T, Nishimoto M, Nomura T (2019) Low mitochondrial DNA variation in the endangered bumble bee Bombus cryptarum florilegus. J Apic Res 58:591–596

    Article  Google Scholar 

  • Tsuchida K, Nagata N, Kojima J (2002) Diploid males and sex determination in paper wasp, Polistes chinensis antennalis (Hymenoptera: Vespidae). Insect Soc 49:12–124

    Article  Google Scholar 

  • Zayed A (2009) Bee genetics and conservation. Apidologie 40:237–262

    Article  Google Scholar 

  • Zayed A, Packer L (2001) High levels of diploid male production in a promitively eusocial bee (Hymenoptera: Halictidae). Heredity 87:631–636

    Article  CAS  PubMed  Google Scholar 

  • Zayed A, Packer L (2005) Complementary sex determination substantially increases extinction proneness of haplodiploid populations. PNAS 102:10742–10746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zayed A, Roubik DW, Packer L (2003) Use of diploid male frequency data as an indicator of pollinator decline. Proc R Soc Lond Ser B Biol Sci 271:S9–S12

    Google Scholar 

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Acknowledgements

This work was supported by JSPS KAKENHI Grant Number 17H03953.

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Authors and Affiliations

  1. Department of Industrial Life Sciences, Faculty of Life Sciences, Kyoto Sangyo University, Kyoto, 603-8555, Japan

    T. Nomura

  2. Laboratory of Animal Breeding and Genetics, Graduate School of Agriculture, Kyoto University, Kyoto, 606-8502, Japan

    Y. Taniguchi

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  1. T. Nomura
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  2. Y. Taniguchi
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Correspondence to T. Nomura.

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Nomura, T., Taniguchi, Y. Simple method for combining multiple-loci marker genotypes to estimate diploid male proportion, with an application to a threatened bumble bee population in Japan. Insect. Soc. 70, 141–147 (2023). https://doi.org/10.1007/s00040-022-00895-z

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  • DOI: https://doi.org/10.1007/s00040-022-00895-z

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