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      Single locus complementary sex determination in Hymenoptera: an "unintelligent" design?

      , 1 , 4 , 2 , 4 , 3 , 4

      Frontiers in Zoology

      BioMed Central

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          Abstract

          The haplodiploid sex determining mechanism in Hymenoptera (males are haploid, females are diploid) has played an important role in the evolution of this insect order. In Hymenoptera sex is usually determined by a single locus, heterozygotes are female and hemizygotes are male. Under inbreeding, homozygous diploid and sterile males occur which form a genetic burden for a population. We review life history and genetical traits that may overcome the disadvantages of single locus complementary sex determination (sl-CSD). Behavioural adaptations to avoid matings between relatives include active dispersal from natal patches and mating preferences for non-relatives. In non-social species, temporal and spatial segregation of male and female offspring reduces the burden of sl-CSD. In social species, diploid males are produced at the expense of workers and female reproductives. In some social species, diploid males and diploid male producing queens are killed by workers. Diploid male production may have played a role in the evolution or maintenance of polygyny (multiple queens) and polyandry (multiple mating). Some forms of thelytoky (parthenogenetic female production) increase homozygosity and are therefore incompatible with sl-CSD. We discuss a number of hypothetical adaptations to sl-CSD which should be considered in future studies of this insect order.

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          The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein.

          Haplodiploid organisms comprise about 20% of animals. Males develop from unfertilized eggs while females are derived from fertilized eggs. The underlying mechanisms of sex determination, however, appear to be diverse and are poorly understood. We have dissected the complementary sex determiner (csd) locus in the honeybee to understand its molecular basis. In this species, csd acts as the primary sex-determining signal with several alleles segregating in populations. Males are hemizygous and females are heterozygous at this locus; nonreproducing diploid males occur when the locus is homozygous. We have characterized csd by positional cloning and repression analysis. csd alleles are highly variable and no transcription differences were found between sexes. These results establish csd as a primary signal that governs sexual development by its allelic composition. Structural similarity of csd with tra genes of Dipteran insects suggests some functional relation of what would otherwise appear to be unrelated sex-determination mechanisms.
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            Complementary sex determination substantially increases extinction proneness of haplodiploid populations.

            The role of genetic factors in extinction is firmly established for diploid organisms, but haplodiploids have been considered immune to genetic load impacts because deleterious alleles are readily purged in haploid males. However, we show that single-locus complementary sex determination ancestral to the haplodiploid Hymenoptera (ants, bees, and wasps) imposes a substantial genetic load through homozygosity at the sex locus that results in the production of inviable or sterile diploid males. Using stochastic modeling, we have discovered that diploid male production (DMP) can initiate a rapid and previously uncharacterized extinction vortex. The extinction rate in haplodiploid populations with DMP is an order of magnitude greater than in its absence under realistic but conservative demographic parameter values. Furthermore, DMP alone can elevate the base extinction risk in haplodiploids by over an order of magnitude higher than that caused by inbreeding depression in threatened diploids. Thus, contrary to previous expectations, haplodiploids are more, rather than less, prone to extinction for genetic reasons. Our findings necessitate a fundamental shift in approaches to the conservation and population biology of these ecologically and economically crucial insects.
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              Animal cytology and evolution

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                Author and article information

                Journal
                Front Zool
                Frontiers in Zoology
                BioMed Central (London )
                1742-9994
                2006
                5 January 2006
                : 3
                : 1
                Affiliations
                [1 ]Department of Zoology, University of Melbourne, VIC 3010 Australia.
                [2 ]Department of Animal Ecology, Institute of Ecological Science, Vrije Universiteit, De Boelelaan 1085, 1081 HV Amsterdam, The Netherlands
                [3 ]Evolutionary Genetics, Centre for Ecological and Evolutionary Studies, University of Groningen, P.O. Box 14, NL-9750 AA Haren, The Netherlands
                [4 ]Institute of Biology Leiden, University of Leiden, P.O. Box 9516, NL-2300 RA Leiden, The Netherlands
                Article
                1742-9994-3-1
                10.1186/1742-9994-3-1
                1360072
                16393347
                Copyright © 2006 van Wilgenburg et al; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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                Animal science & Zoology

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