Haplodiploidy

The haplodiploid sex-determination system determines the sex of the offspring of many hymenopterans (bees, ants, and wasps), spider mites, coleopterans (bark beetles) and rotifers. In this system, sex is determined by the number of sets of chromosomes an individual receives. An offspring formed from the union of a sperm and an egg develops as a female, and an unfertilized egg develops as a male. This means that the males have half the number of chromosomes that a female has, and are haploid. This haplodiploid sex-determination system produces a number of peculiarities; chief among these is that a male has no father and cannot have sons, but he has a grandfather and can have grandsons. Haplodiploidy is postulated as having paved the way for the evolution of eusociality in the Hymenoptera and a few other taxa although this is a matter of considerable debate.^[1] ^[2]

Mechanisms

Several models have been proposed for the genetic mechanisms of haplodiploid sex-determination. The model most commonly referred to is the complementary allele model. According to this model, if an individual is heterozygous for a certain locus, it develops into a female, whereas hemizygous and homozygous individuals develop into males. In other words, diploid offspring develop from fertilized eggs, and are normally female, while haploid offspring develop into males from unfertilized eggs. Diploid males would be infertile, as their cells would not undergo meiosis to form sperm. Therefore the sperm would be diploid, which means that their offspring would be triploid. Since hymenopteran mother and sons share the same genes they may be especially sensitive to inbreeding: Inbreeding reduces the number of different sex alleles present in a population, hence increasing the occurrence of diploid males.

After mating, fertile Hymenopteran females store the sperm in an internal sac called the spermatheca. The mated female controls the release of stored sperm from within the organ: If she releases sperm as an egg passes down the oviduct, the egg is fertilized. ^[3] Social bees, wasps, and ants can modify sex ratios within colonies to maximize relatedness among members, and to generate a workforce appropriate to surrounding conditions. ^[4]

Sex-determination in honey bees

In honeybees the drones (males) are entirely derived from the queen, their mother. The diploid queen has 32 chromosomes and the haploid drones have 16 chromosomes. Drones produce sperm cells that contain their entire genome, so the sperm are all genetically identical except for mutations. The genetic makeup of the female worker bees is half derived from the mother, and half from the father, but the male bees' genetic makeup is entirely derived from the mother.^[5] Thus, if a queen bee mates with only one drone, any two of her daughters will share, on average, 3/4 of their genes. The diploid queen's genome is recombined for her daughters, but the haploid father's genome is inherited by his daughters "as is".

While workers can lay unfertilized eggs that become their sons, haplodiploid sex-determination system is beneficial to the individual due to indirect selection. Since the worker is more related to the queen's daughters (her sisters) than to her own offspring, helping the queen's offspring to survive aids the spread of the same genes that the worker possesses more efficiently than direct reproduction. ^[6] Batches of worker bees are short lived and are constantly being replaced by the next batch, so this kin selection is possibly a strategy to ensure the proper working of the hive. However, since queens usually mate with a dozen drones or more, not all workers are full sisters. Due to the separate storage of drone sperm, a specific batch of brood may be more closely related than a specific batch of brood laid at a later date.

Relatedness ratios in haplodiploid

Relatedness is used to calculate the strength of kin selection (via Hamilton's rule). The haplodiploidy hypothesis states that the unusual 3/4 relatedness coefficient amongst full haplodiploid sisters is responsible for the frequency of evolution of eusocial behavior in hymenoptera.^[7]

Relatedness coefficients in haplodiploid organisms are as follows.

**Shared gene proportions in haplo-diploid sex-determination system relationships**
Sex	Daughter	Son	Mother	Father	Full Sister	Full Brother
Female	1/2	1	1/2	1/2	3/4	1/4
Male	1/2	N/A	1	N/A	1/2	1/2

Controversy

The haplodiploidy hypothesis is often given as a clear example of kin selection.^[2] Since full hymenopteran sisters share more genes than a parent shares with its offspring, it follows that helping to rear sisters should be favored over having children as an evolutionary strategy. However, this argument neglects that eusocial drones help raise their brothers in addition to their sisters, which, given the typical sex ratio of 1:1, results in raising siblings with an average relatedness coefficient of 1/2, which is no better than that of young.^[7] Ratios can be even lower in colonies where the queen has mated with multiple males, which is common in some species.^[8] This, combined with the discovery of multiple diploid eusocial organisms and at least one haplodiploid eusocial species with a male nonreproductive caste, has been referred to by one of the founding figures of sociobiology, E. O. Wilson, as the "collapse of the haplodiploid hypothesis".^[2] However, not all researchers believe the hypothesis has been disproven, and evidence continues to be collected on both sides. Statistical analysis suggests that in each of the independent evolutions of eusociality, queens mated with only one male,^[8] which suggests having highly related offspring was important. Furthermore, often the female bees give more food to the females than to the males, and in times of dearth they even kill the males.

References

Notes

^ William O. H. Hughes, Benjamin P. Oldroyd, Madeleine Beekman, Francis L. W. Ratnieks (2008-05-30). "Ancestral Monogamy Shows Kin Selection Is Key to the Evolution of Eusociality". Science. 320 (5880). American Association for the Advancement of Science: 1213–1216. doi:10.1126/science.1156108. PMID 18511689. Retrieved 2008-08-04.{{cite journal}}: CS1 maint: multiple names: authors list (link)
^ ^a ^b ^c Edward O. Wilson (2005-09-12). "Kin selection as the key to altruism: its rise and fall" (PDF). Social Research. 72: 1–8. Retrieved 2011-03-25.
^ van Wilgenburg, Ellen; Driessen, Gerard & Beukeboom, Leo W. Single locus complementary sex determination in Hymenoptera: an "unintelligent" design? Frontiers in Zoology 2006, 3:1
^ Mahowald, Michael; von Wettberg, Eric Sex determination in the Hymenoptera Swarthmore College (1999)
^ Sinervo, Barry Kin Selection and Haplodiploidy in Social Hymenoptera 1997
^ Foster, Kevin R.; Ratnieks, Francis L. W. The Effect of Sex-Allocation Biasing on the Evolution of Worker Policing in Hymenopteran Societies The American Naturalist, volume 158 (2001), pages 615–623
^ ^a ^b Kevin R. Foster, Tom Wenseleers and Francis L.W. Ratnieks (2006). "Kin selection is the key to altruism". Trends in ecology & evolution. 21 (2). Elsevier: 57–60. doi:10.1016/j.tree.2005.11.020.
^ ^a ^b Hughes, W. O. H., and Oldroyd, B. P., and Beekman, M., and Ratnieks, F. L. W. (2008). "Ancestral monogamy shows kin selection is key to the evolution of eusociality". Science. 320 (5880). American Association for the Advancement of Science: 1213. doi:10.1126/science.1156108. ISSN 0036-8075. PMID 18511689. {{cite journal}}: no-break space character in |author= at position 8 (help)CS1 maint: multiple names: authors list (link)

Bibliography

Beye, Martin; Hunt, Greg J. ; Page, Robert E. ; Fondrk, M. Kim; Grohmann, Lore and Moritz, R. F. A. Unusually High Recombination Rate Detected in the Sex Locus Region of the Honey Bee (Apis mellifera) Genetics, Vol. 153, 1701-1708, December 1999
Wu, Z.; Hopper, K. R.; Ode, P. J. ; Fuester, R. W.; Tuda, M., and Heimpel, G. E. Single-locus complementary sex determination absent in Heterospilus prosopidis (Hymenoptera: Braconidae) Heredity (2005) 95, 228–234
Ratnieks, Francis Reproductive harmony via mutual policing by workers in eusocial hymenoptera American Naturalist 132(2) 217-236 ; 1988

[0-1] William O. H. Hughes, Benjamin P. Oldroyd, Madeleine Beekman, Francis L. W. Ratnieks (2008-05-30). "Ancestral Monogamy Shows Kin Selection Is Key to the Evolution of Eusociality". Science. 320 (5880). American Association for the Advancement of Science: 1213–1216. doi:10.1126/science.1156108. PMID 18511689. Retrieved 2008-08-04.{{cite journal}}: CS1 maint: multiple names: authors list (link)

[eowilson-2] Edward O. Wilson (2005-09-12). "Kin selection as the key to altruism: its rise and fall" (PDF). Social Research. 72: 1–8. Retrieved 2011-03-25.

[3] van Wilgenburg, Ellen; Driessen, Gerard & Beukeboom, Leo W. Single locus complementary sex determination in Hymenoptera: an "unintelligent" design? Frontiers in Zoology 2006, 3:1

[4] Mahowald, Michael; von Wettberg, Eric Sex determination in the Hymenoptera Swarthmore College (1999)

[5] Sinervo, Barry Kin Selection and Haplodiploidy in Social Hymenoptera 1997

[6] Foster, Kevin R.; Ratnieks, Francis L. W. The Effect of Sex-Allocation Biasing on the Evolution of Worker Policing in Hymenopteran Societies The American Naturalist, volume 158 (2001), pages 615–623

[kiniskey-7] Kevin R. Foster, Tom Wenseleers and Francis L.W. Ratnieks (2006). "Kin selection is the key to altruism". Trends in ecology & evolution. 21 (2). Elsevier: 57–60. doi:10.1016/j.tree.2005.11.020.

[hughes2008ancestral-8] Hughes, W. O. H., and Oldroyd, B. P., and Beekman, M., and Ratnieks, F. L. W. (2008). "Ancestral monogamy shows kin selection is key to the evolution of eusociality". Science. 320 (5880). American Association for the Advancement of Science: 1213. doi:10.1126/science.1156108. ISSN 0036-8075. PMID 18511689. {{cite journal}}: no-break space character in |author= at position 8 (help)CS1 maint: multiple names: authors list (link)

[1]

[2]

[3]

[4]

[5]

[6]

[7]

[8]