Spermatogenesis in Diploid Drones of the Honeybee

Woyke, J.; Skowronek, W.

doi:10.1080/00218839.1974.11099777

Cited by 23 publications

(9 citation statements)

References 10 publications

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“…Consequently, our results bring into question widespread assumptions about the inability of diploid males to reproduce. Investigations of sperm production in haploid male hymenopterans have shown that spermatogenesis begins with a reductional division (meiosis I) that is aborted during metaphase I (18,44,45). The diploid sperm made by diploid males of other species (10,16,17,19) is presumably the result of these same events occurring even when two complementary sets of chromosomes are present in the spermatogonium.…”

Section: Discussionmentioning

confidence: 99%

“…In a number of species, diploid males have normal viability (6,10,11) but fail to pass their genetic material to subsequent generations because they are unable to mate properly (12) or because they are sterile (13)(14)(15)(16). Some diploid males have been shown to produce viable sperm, but this sperm is diploid rather than haploid and results in sterile triploid progeny (10,12,(17)(18)(19). The picture that has emerged regarding diploid males is that they perform poorly across a variety of traits associated with fitness, and should they succeed in fathering any surviving offspring, these offspring will themselves be incapable of reproducing.…”

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confidence: 99%

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Functionally reproductive diploid and haploid males in an inbreeding hymenopteran with complementary sex determination

Cowan

Stahlhut

2004

Proc. Natl. Acad. Sci. U.S.A.

104

120

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It has become a matter of orthodoxy that among wasps, ants, bees, and other insects in the order Hymenoptera, only uniparental haploid males that arise from unfertilized eggs are capable of reproduction. This idea is of interest because the best understood and perhaps most widespread sex determination system among these insects [known as single locus complementary sex determination (sl-CSD)] does not depend on ploidy alone and, paradoxically, consistently results in small numbers of diploid biparental males. To date, the reproductive potential of diploid males has been studied in 13 of the perhaps 200,000 hymenopterans worldwide; in each of these instances, the diploid males are genetic dead ends because they are inviable or sterile. The data from these species have resulted in a general conclusion that has been invoked for virtually all species with sl-CSD and has become the basis for assumptions regarding conservation biology, sex ratio analysis, and the evolution of social behavior. Here, we report that in the solitary vespid wasp Euodynerus foraminatus, both diploid and haploid males are fertile, which documents normal fertility in diploid males of a hymenopteran with sl-CSD. This wasp has high levels of inbreeding because of frequent brother-sister mating in nature; therefore, diploid males are more frequently produced and thus more likely exposed to selection favoring their fertility. Because inbreeding and diploid male production may be important features of the population biology of many hymenopterans, we sound a cautionary note regarding ideas about the evolutionary ecology of these insects.

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

Functionally reproductive diploid and haploid males in an inbreeding hymenopteran with complementary sex determination

Cowan

Stahlhut

2004

Proc. Natl. Acad. Sci. U.S.A.

104

120

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“…The haploidy and diploidy of the adults were confirmed following the dissection of the males and the visual inspection of their testes under a stereomicroscope. It is known that 2n males have smaller testes compared with those of n males (WOYKE & SKOWRONEK 1974, DUCHATEAU & MARIËN 1995.…”

Section: Shortmentioning

confidence: 99%

Digestive and regenerative cells in the midgut of haploid and diploid males of the stingless bee Melipona quadrifasciata anthidioides (Hymenoptera: Apidae)

Fernandes¹,

Martins²,

Serrão³

et al. 2012

Zoologia (Curitiba)

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In eusocial bees, workers and queens are diploid (2n), whereas males are haploid (n). However, in some species, including the stingless bee Melipona quadrifasciata anthidioides Lepeletier, 1836, 2n males arise from fertilized eggs resulting from the crossing between a queen and her brother. In the present study, we provide a comparative analysis of the digestive and regenerative cells in n and 2n pupae and adult males of M. quadrifasciata anthidioides. In n and 2n pupae and adult males, the number of regenerative cells/nest was similar. In n and 2n pupae, the mean number of digestive cells/midgut area was 2076 ± 0.60, whereas in adults it was 1234 ± 1.42 digestive cells/midgut area. The nuclear area of the digestive cells was also similar in both n and 2n adult males (~154 µm²) and smaller in pupae (~91 µm²); this variation might be a result of DNA amplification in digestive cells during bee development. The results from our current study provide further understanding of the morphological and physiological aspects of the digestive tract of bees and show that the ploidy difference between n and 2n male stages does not affect the number of digestive and regenerative cells in the midgut of M. quadrifasciata anthidioides

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“…They may have low viability (Whiting, 1943;Petters and Mettus, 1980), may survive but be unable to mate (Smith and Wallace, 1971), or may be sterile (Cook, 1993b;Krieger et al, 1999). Spermatogenesis in male hymenopterans generally does not include a reductional division (Hogge and King, 1975); consequently, diploid males in some species are known to produce abnormal diploid sperm (Woyke and Skowronek, 1974;Yamauchi et al, 2001), which, if capable of fertilization, results in sterile triploid offspring (Inaba, 1939;Smith and Wallace, 1971;Krieger et al, 1999). The fitness of diploid males is therefore expected to be zero.…”

Section: Introductionmentioning

confidence: 99%

Single-locus complementary sex determination in the inbreeding wasp Euodynerus foraminatus Saussure (Hymenoptera: Vespidae)

Stahlhut

Cowan

2003

Heredity

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The Hymenoptera have arrhenotokous haplodiploidy in which males normally develop from unfertilized eggs and are haploid, while females develop from fertilized eggs and are diploid. Multiple sex determination systems are known to underlie haplodiploidy, and the best understood is singlelocus complementary sex determination (sl-CSD) in which sex is determined at a single polymorphic locus. Individuals heterozygous at the sex locus develop as females; individuals that are hemizygous (haploid) or homozygous (diploid) at the sex locus develop as males. sl-CSD can be detected with inbreeding experiments that produce diploid males in predictable proportions as well as sex ratio shifts due to diploid male production. This sex determination system is considered incompatible with inbreeding because the ensuing increase in homozygosity increases the production of diploid males that are inviable or infertile, imposing a high cost on matings between close relatives. However, in the solitary hunting wasp Euodynerus foraminatus, a species suspected of having sl-CSD, inbreeding may be common due to a high incidence of sibling matings at natal nests. In laboratory crosses with E. foraminatus, we find that sex ratios and diploid male production (detected as microsatellite heterozygosity) are consistent with sl-CSD, but not with other sex determination systems. This is the first documented example of sl-CSD in a hymenopteran with an apparent natural history of inbreeding, and thus presents a paradox for our understanding of hymenopteran genetics.

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Spermatogenesis in Diploid Drones of the Honeybee

Cited by 23 publications

References 10 publications

Functionally reproductive diploid and haploid males in an inbreeding hymenopteran with complementary sex determination

Functionally reproductive diploid and haploid males in an inbreeding hymenopteran with complementary sex determination

Digestive and regenerative cells in the midgut of haploid and diploid males of the stingless bee Melipona quadrifasciata anthidioides (Hymenoptera: Apidae)

Single-locus complementary sex determination in the inbreeding wasp Euodynerus foraminatus Saussure (Hymenoptera: Vespidae)

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