Bee genetics and conservation Amro Zayed To cite this version: Amro Zayed. Bee genetics and conservation. Apidologie, Springer Verlag, 2009, 40 (2), 10.1051/apido/2009026. hal-00892012 HAL Id: hal-00892012 https://hal.archives-ouvertes.fr/hal-00892012 Submitted on 1 Jan 2009 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Apidologie 40 (2009) 237–262 Available online at: c INRA/DIB-AGIB/EDP Sciences, 2009 www.apidologie.org DOI: 10.1051/apido/2009026 Review article Bee genetics and conservation* Amro Zayed Institute for Genomic Biology, University of Illinois at Urbana-Champaign, 1206 West Gregory Drive, Urbana, 61801, USA Received 29 August 2008 – Revised 5 January 2009 – Accepted 15 January 2009 Abstract – The emerging threat of pollinator decline has motivated research on bee conservation biology in order to both understand the causes of declines and to develop appropriate conservation strategies. The ap- plication of genetics to the conservation of diploid animals has proven to be important for both overcoming genetic threats to population viability and for providing tools to guide conservation programs. However, the haplodiploid bees have several unusual genetic properties of relevance to their conservation, which warrant special attention. Here I review how haplodiploidy and complementary sex determination affect genetic parameters pertinent to the viability and future evolutionary potential of bee populations. I also review how genetic tools can improve the conservation management of bees. I find that bees are especially prone to extinction for genetic reasons, and that genetics can provide invaluable tools for managing bee populations to circumvent pollinator decline. haplodiploid / complementary sex determination / inbreeding depression / diploid males / extinction 1. INTRODUCTION purpose of examining the causes of pollinator decline and developing appropriate conserva- There are nearly 20,000 known species of tion strategies to circumvent it (e.g. Dias et al., bees worldwide (Michener, 2000), and they 1999;Kremenetal.,2007; NRC, 2007; Byrne are integral components of terrestrial ecosys- and Fitzpatrick, 2009). tems due to their indispensable role as pol- linators (Allen-Wardell et al., 1998; Klein Several extrinsic factors have been pro- et al., 2007;Kremenetal.,2007). Over the posed to explain the observed declines in past decade, multiple lines of evidence have bee populations: habitat fragmentation and shown that both native and managed pollina- loss, agricultural intensification, overuse of tors are experiencing a seemingly world-wide pesticides, pathogen spill-over from managed decline (Biesmeijer et al., 2006; Fitzpatrick pollinators, invasive species, and global cli- et al., 2006;Kosioretal.,2007; NRC, 2007; mate change (Cane, 2001; Cane and Tepedino, Colla and Packer, 2008;Goulsonetal.,2008; 2001;Kremenetal.,2002; Müller et al., Grixti et al., 2009), fueling both ecological 2006; NRC, 2007;Murrayetal.,2009). and economic concerns (Kremen et al., 2002; Genetic aspects of bee declines were com- Fontaine et al., 2006;Vamosietal.,2006; pletely neglected in the early syntheses (e.g. Olesen et al., 2007;Pauw,2007). This emerg- Dias et al., 1999) despite the overwhelming ing threat has mobilized the academic commu- evidence that genetic factors can play im- nity through the establishment of international portant roles in species extinction (Saccheri research initiatives and partnerships with the et al., 1998; Frankham et al., 2002;Spielman et al., 2004; Hanski and Saccheri, 2006). Corresponding author: A. Zayed, Several factors likely contributed to the ini- [email protected] tial oversight of possible genetic aspects of * Manuscript editor: Robert Paxton bee declines, including: (1) Prior theoretical Article published by EDP Sciences 238 A. Zayed arguments suggesting that genetics is rela- plausible and best supported genetic threats to tively unimportant in the conservation biol- the viability of small bee populations: Com- ogy of haplodiploids (Box I). (2) Difficulties in plementary sex determination, inbreeding de- extrapolating knowledge gained from diploid pression, and loss of genetic diversity and con- organisms to the haplodiploid bees. (3) Lack sequent evolutionary potential. I do not discuss of studies examining how specific bee genetic the hypothesized effects of the accumulation and life history traits (e.g. haplodiploidy, com- of deleterious mutations on population vi- plementary sex determination, sociality, etc.) ability (Lynch et al., 1995), given limited impact population viability. (4) Lack of ge- empirical support of ‘mutational meltdowns’ netic resources for bees. However, theoretical in sexually-reproducing populations (reviewed and technical advances over the past decade by Frankham, 2005). Box I contains a glos- have overturned longstanding views regard- sary of terms relevant to bee conservation ge- ing the immunity of bees to genetic threats in netics. The terminology relating to inbreeding small populations and prompted research on is historically a very murky subject (Jacquard, their conservation genetics. 1975; Templeton and Read, 1994; Keller and Research in conservation genetics can be Waller, 2002). Following Glémin (2003)and conceptually divided into two general types Leberg and Firmin (2008), here I use ‘sys- of inquiry: (1) How does genetics contribute tematic inbreeding’ to describe species with to population decline and extinction? (2) How mating systems characterized by ‘inbreeding’ can molecular tools be utilized to learn about (Box I). I use inbreeding by drift to de- an organism’s characteristics relevant to con- scribe the increasing probability of relatedness servation and management (e.g. taxonomy, among mates in small populations (Box I). The natural history, and demography)? In this re- term inbreeding depression (Box I) can also view, I summarize and synthesize studies on be ambiguous. Defined broadly, inbreeding de- how genetics can contribute to bee declines pression, or reduced fitness of inbred individ- (Sect. 2), focusing on how haplodiploidy and uals, can encompass the effects of comple- genetic sex determination affect parameters mentary sex determination that are unique to relevant to population viability and evolution- some members of the Hymenoptera. However, ary potential. I also review how genetic and inbreeding depression is classically ascribed genomic tools can be used in conservation to dominance and overdominance (Box I) – and management of bee populations (Sect. 3). which are common to both diploids and hap- To ensure that my review is accessible to lodiploids. Here I treat the unique effects of the largest possible readership, I focus on complementary sex determination on the fit- presenting general concepts without delving ness of haplodiploids as distinct from inbreed- into detailed mathematical treatments. For the ing depression caused by dominance and over- mathematically inclined, I recommend several dominance. reviews on haplodiploid population genetics (Crozier, 1977; Hedrick and Parker, 1997), and conservation genetics (Frankham et al., 2002; 2.1. Complementary sex determination Gaggiotti, 2003; Hedrick, 2004; Frankham, and bee declines: death by diploidy 2005). Bees belong to the insect order Hy- menoptera, a group characterized by hap- 2. GENETIC ASPECTS OF BEE lodiploidy (i.e. Females are diploid while DECLINES males are usually haploid; Box I). The pre- sumed ancestral sex determination mechanism Genetic threats can reduce the viability of in the Hymenoptera is single locus comple- small wildlife populations over the short term mentary sex determination (sl-CSD; Box I), by reducing fitness, as well as over the long where sex is determined by genotype at a term by limiting evolutionary potential (Box I) single gene (Cook, 1993; van Wilgenburg and adaptability. Here I discuss the three most et al., 2006; Heimpel and de Boer, 2008). Bee conservation genetics 239 Ayabe et al., 2004; Liebert et al., 2004, 2005), with one rare exception in an aculeate wasp (Cowan and Stahlhut, 2004). In such cases, the production of diploid males indirectly in- creases female mortality by constraining their mates to the production of haploid males and triploid daughters. Therefore, diploid male production increases female mortality over one or two generations, given inviable or ef- Figure 1. Diploid male production. A matched mat- fectively sterile diploid males respectively. Ul- ing results when a female mates with a male shar- timately, increased female mortality caused by ing a sex-determining allele in common (allele E). diploid male production will result in reduced Half of the female’s diploid progeny – all intended population growth rates in bee populations to be female – will be homozygous at the sex deter- mination locus and will develop into diploid males (Stouthamer et al., 1992; Pamilo and Crozier, (genotype EE). 1997). In social bees, diploid male production will effectively increase female mortality for both reproductive and worker castes, and can Heterozygotes