Haplodiploidy

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In the Hymenoptera, the sex-determination system involves haploid males and diploid females. System for honey bee shown. Haplodiploid Sex Determination in Honey Bees.svg
In the Hymenoptera, the sex-determination system involves haploid males and diploid females. System for honey bee shown.

Haplodiploidy is a sex-determination system in which males develop from unfertilized eggs and are haploid, and females develop from fertilized eggs and are diploid. [1] Haplodiploidy is sometimes called arrhenotoky.

Contents

Haplodiploidy determines the sex in all members of the insect orders Hymenoptera (bees, ants, and wasps) [2] and Thysanoptera ('thrips'). [3] The system also occurs sporadically in some spider mites, Hemiptera, Coleoptera (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.

The haplodiploid sex-determination system has a number of peculiarities. For example, a male has no father and cannot have sons, but he has a grandfather and can have grandsons. Additionally, if a eusocial-insect colony has only one queen, and she has only mated once, then the relatedness between workers (diploid females) in a hive or nest is 34. This means the workers in such monogamous single-queen colonies are significantly more closely related than in other sex determination systems where the relatedness of siblings is usually no more than 12. It is this point which drives the kin selection theory of how eusociality evolved. [4] Whether haplodiploidy did in fact pave the way for the evolution of eusociality is still a matter of debate. [5] [6]

Another feature of the haplodiploidy system is that recessive lethal and deleterious alleles will be removed from the population rapidly because they will automatically be expressed in the males (dominant lethal and deleterious alleles are removed from the population every time they arise, as they kill any individual they arise in). [3]

Haplodiploidy is not the same thing as an X0 sex-determination system. In haplodiploidy, males receive one half of the chromosomes that females receive, including autosomes. In an X0 sex-determination system, males and females receive an equal number of autosomes, but when it comes to sex chromosomes, females will receive two X chromosomes while males will receive only a single X chromosome.

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, each fertile hymenopteran female stores 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 her oviduct, the egg is fertilized. [7] Social bees, wasps, and ants can modify sex ratios within colonies which maximizes relatedness among members and generates a workforce appropriate to surrounding conditions. [8] In other solitary hymenopterans, the females lay unfertilized male eggs on poorer food sources while laying the fertilized female eggs on better food sources, possibly because the fitness of females will be more adversely affected by shortages in their early life. [9] [10] Sex ratio manipulation is also practiced by haplodiploid ambrosia beetles, who lay more male eggs when the chances for males to disperse and mate with females in different sites are greater. [11]

Sex determination in honey bees

Honey bee workers are unusually closely related to their full sisters (same father) because of their haplodiploid inheritance system. Apis mellifera (queen and workers).jpg
Honey bee workers are unusually closely related to their full sisters (same father) because of their haplodiploid inheritance system.

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 male bees' genetic makeup is therefore entirely derived from the mother, while the genetic makeup of the female worker bees is half derived from the mother, and half from the father. [12] Thus, if a queen bee mates with only one drone, any two of her daughters will share, on average, 34 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". It is also possible for a laying worker bee to lay an unfertilised egg, which is always a male.

There are rare instances of diploid drone larvae. This phenomenon usually arises when there is more than two generations of brother-sister mating. [13] Sex determination in honey bees is initially due to a single locus, called the complementary sex determiner (csd) gene. In developing bees, if the conditions are that the individual is heterozygous for the csd gene, they will develop into females. If the conditions are so that the individual is hemizygous or homozygous for the csd gene, they will develop into males. The instances where the individual is homozygous at this gene are the instances of diploid males. [14] Diploid males do not survive to adulthood, as the nurse worker bees will cannibalize the diploid males upon hatching. [15]

While workers can lay unfertilized eggs that become their sons, haplodiploid sex-determination system increases the individual's fitness 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 helps the spread of the same genes that the worker possesses more efficiently than direct reproduction. [16]

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. However, many other species of bees, including bumblebees, such as Bombus terrestris , are monandrous. [17] This means that sisters are almost always more related to one another than they would be to their own offspring, thus eliminating the conflict of variable relatedness present in honeybees. [18]

Sex determination in chalcidoid wasps

In wasps of the genus Nasonia , a non-CSD method of sex determination has been documented. The most recent accepted model for this non-CSD system is called Maternal Effect Genomic Imprinting Sex Determination (MEGISD). This model involves a masculinizing/virilizing maternal effect gene that “imprints upon” the cytoplasmic component of oocytes, and an “unimprinted” paternal contribution (in female offspring) that provides a counter effect to virilization and allows for female development to occur. Since all diploid eggs become female (due to the factor originating in the male genetic contribution that prevents masculinization), this differs from CSD in that under CSD, diploid eggs can become males if they are homozygous or hemizygous. [19]

Relatedness ratios in haplodiploidy

Relatedness is used to calculate the strength of kin selection (via Hamilton's rule). [20] The haplodiploidy hypothesis proposes that the unusual 34 relatedness coefficient amongst full haplodiploid sisters is responsible for the frequency of evolution of eusocial behavior in hymenopterans. [21] A eusocial worker helping her mother birth more sisters propagates more of her own genes than had she reproduced herself.

In normal sexual reproduction, the father has two sets of chromosomes, and crossing over takes place between the chromatids of each pair during the meiosis which produces the sperm. Therefore, the sperms are not identical, because in each chromosome of a pair there will be different alleles at many of the loci. But when the father is haploid all the sperms are identical (except for a small number where gene mutations have taken place in the germ line). So, all female offspring inherit the male's chromosomes 100% intact. As long as a female has mated with only one male, all her daughters share a complete set of chromosomes from that male. In Hymenoptera, the males generally produce enough sperm to last the female for her whole lifetime after a single mating event with that male. [20]

Relatedness coefficients in haplodiploid organisms are as follows, assuming that a female has only mated once. These ratios apply, for example, throughout a bee hive, unless some laying workers produce offspring, which will all be males from unfertilised eggs: in that case, average relatedness will be lower than shown.

Shared gene proportions in haplo-diploid sex-determination system relationships
SexFemaleMale
Daughter121
Son12
Mother121
Father12
Sister3412
Brother1412
Maternal Aunt3834
Maternal Uncle1814
Paternal Aunt14
Paternal Uncle14
Niece (sister's daughter)3814
Niece (brother's daughter)1412
Nephew (sister's son)3814

Under this assumption that mothers only mate once, sisters are more strongly related to each other than to their own daughters. This fact has been used to explain the evolution of eusociality in many hymenopterans. However, colonies which have workers from multiple queens or queens which have mated multiple times will have worker-to-worker relatedness which is less than worker-to-daughter relatedness, such as in Melipona scutellaris .

See also

Related Research Articles

is the process of male gamete formation in animals This process also involves

<span class="mw-page-title-main">Hymenoptera</span> Order of insects comprising sawflies, wasps, bees, and ants

Hymenoptera is a large order of insects, comprising the sawflies, wasps, bees, and ants. Over 150,000 living species of Hymenoptera have been described, in addition to over 2,000 extinct ones. Many of the species are parasitic. Females typically have a special ovipositor for inserting eggs into hosts or places that are otherwise inaccessible. This ovipositor is often modified into a stinger. The young develop through holometabolism —that is, they have a wormlike larval stage and an inactive pupal stage before they mature.

<span class="mw-page-title-main">Sex</span> Trait that determines an organisms sexually reproductive function

Sex is the trait that determines whether a sexually reproducing organism produces male or female gametes. A male organism produces small mobile gametes, while a female organism produces larger, non-mobile gametes. An organism that produces both types of gamete is called a hermaphrodite. During sexual reproduction, a male and a female gamete fuse to form a zygote, which develops into an offspring that inherits traits from each parent.

<span class="mw-page-title-main">Sex-determination system</span> Biological system that determines the development of an organisms sex

A sex-determination system is a biological system that determines the development of sexual characteristics in an organism. Most organisms that create their offspring using sexual reproduction have two common sexes and a few less common intersex variations.

<i>Formica exsecta</i> Species of ant

Formica exsecta is a species of ant found from Western Europe to Asia.

<span class="mw-page-title-main">Drone (bee)</span> Male bee

A drone is a male bee. Unlike the female worker bee, a drone has no stinger. He does not gather nectar or pollen and cannot feed without assistance from worker bees. His only role is to mate with a maiden queen in nuptial flight.

<span class="mw-page-title-main">Arrhenotoky</span> Male-producing form of parthenogenesis

Arrhenotoky, also known as arrhenotokous parthenogenesis, is a form of parthenogenesis in which unfertilized eggs develop into males. In most cases, parthenogenesis produces exclusively female offspring, hence the distinction.

<i>Bombus ternarius</i> Species of insect

Bombus ternarius, commonly known as the orange-belted bumblebee or tricolored bumblebee, is a yellow, orange and black bumblebee. It is a ground-nesting social insect whose colony cycle lasts only one season, common throughout the northeastern United States and much of Canada. The orange-belted bumblebee forages on Rubus, goldenrods, Vaccinium, and milkweeds found throughout the colony's range. Like many other members of the genus, Bombus ternarius exhibits complex social structure with a reproductive queen caste and a multitude of sister workers with labor such as foraging, nursing, and nest maintenance divided among the subordinates.

<span class="mw-page-title-main">Parthenogenesis</span> Asexual reproduction without fertilization

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<i>Nasonia vitripennis</i> Species of insect

Nasonia vitripennis is one of four known species under the genus Nasonia - small parasitoid wasps that afflict the larvae of parasitic carrion flies such as blowflies and flesh flies, which themselves are parasitic toward nestling birds. It is the best known and most widely studied of the parasitoid wasps, and their study forms a vital part of the information used to describe the order Hymenoptera, along with information from bees and ants. This parasitoid behaviour makes the wasps an interest for the development of biopesticide and biological systems for controlling unwanted insects.

<span class="mw-page-title-main">Eusociality</span> Highest level of animal sociality a species can attain

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<i>Austroplatypus incompertus</i> Species of beetle

Austroplatypus incompertus is a species of ambrosia beetle belonging to the true weevil family, native to Australia, with a verified distribution in New South Wales and Victoria. It forms colonies in the heartwood of Eucalyptus trees and is the first beetle to be recognized as a eusocial insect. Austroplatypus incompertus is considered eusocial because groups contain a single fertilized female that is protected and taken care of by a small number of unfertilized females that also do much of the work. The species likely passed on cultivated fungi to other weevils.

<span class="mw-page-title-main">Evolution of eusociality</span> Origins of cooperative brood care

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<i>Lasioglossum zephyrus</i> Species of bee

Lasioglossum zephyrus is a sweat bee of the family Halictidae, found in the U.S. and Canada. It appears in the literature primarily under the misspelling "zephyrum". It is considered a primitively eusocial bee, although it may be facultatively solitary. The species nests in burrows in the soil.

Pseudo-arrhenotoky or paternal genome elimination is the phenomenon where males develop from fertilized eggs but the paternal genome is heterochromatinized or lost in the somatic cells and not passed on to their offspring.

<span class="mw-page-title-main">Worker policing</span> Insects destroying eggs not laid by queen

Worker policing is a behavior seen in colonies of social hymenopterans whereby worker females eat or remove eggs that have been laid by other workers rather than those laid by a queen. Worker policing ensures that the offspring of the queen will predominate in the group. In certain species of bees, ants and wasps, workers or the queen may also act aggressively towards fertile workers. Worker policing has been suggested as a form of coercion to promote the evolution of altruistic behavior in eusocial insect societies.

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<i>Melipona scutellaris</i> Species of bee

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<i>Bombus ignitus</i> Species of bee

Bombus ignitus is a species of bumblebee in the family Apidae. It is mainly distributed in Eastern Asia, commonly found in China, Japan and Korea. It is used in China and Japan commercially as a pollinator. B. ignitus is a eusocial insect with a queen that is monandrous: mating with only one male in the late summer before hibernating until the following spring. It builds its nest out of a mass of pollen and lays its eggs after completion. Due to numerous conflicts between queens and fertile workers, some surviving queens are badly injured, described by some as living corpses.

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