Advantages of sex

Set against the cost of sex, particularly the cost of males, sex has three distinct advantages over asexual methods of reproduction, conferred by genetic recombination and cross fertilisation. These are (1) to bring together in the same individual mutations arising in different individuals (Muller's ratchet); (2) to shuffle genes in every generation and thus keep parasites at bay (Red Queen hypothesis); (3) to generate genetic variability and thus to adapt to changing environments. These advantages act over evolutionary time-scales, yet sex has an immediate two-fold cost, given by its requirement for males. If an asexual mutant species arising from a sexual population is inherently less variable than its ancestral species then we can add an immediate ecological advantage of sex, that it generates a wider niche and/or competitive advantage. Niche width or dominance may be sufficient to prevent establishment by the asexual, or it may allow coexistence between the two forms (Tangled Bank and Frozen Niche Variation hypotheses).

Agamic generation

A generation that comprises parthenogenetically reproducing females that are genetically diploid. They lay unfertilised eggs that may be male (having undergone meiosis) or female (having not undergone meiosis). In the gall wasps (Cynipidae) agamic females emerge from over-wintering in protective galls.

Agamospermy

Asexual reproduction in plants other than by vegetative propagation (equivalent to parthenogenesis in animals).

Allee effect

Reduced reproductive success at low density, due to difficulty of finding mates.

Allele

A variant of a single gene, inherited at a particular genetic locus.

Allozyme

Variant form of an enzyme (protein) that results from the presence of different alleles for the gene that produces the enzyme.

Ameiotic parthenogenesis

Parthenogenesis without pairing of homologous chromosomes and usually with only a single maturation division occurring in the oocyte during oogenesis, by mitosis. This is the reproductive mode of polyploid forms of the Enchytraeid worm Lumbricillus lineatus, but is otherwise rare amongst annelids.

Amphimixis

True sexual reproduction, involving the fusion of male and female gametes and the formation of a zygote.

Anisogamy

Sexual reproduction involving production of gametes that differ in size, and often function. For example in conventional sexual reproduction in animals, a mobile male spermatozoon fertilises an immobile female ovum, which develops the new offspring. Sexual reproduction in yeast in contrast is isogamous, with both sexes producing offspring.

Aphallic

Hermaphrodites without male phallus, i.e. obligate females amongst hermaphrodites.

Apomict

Asexually reproducing individual.

Apomixis

Asexual reproduction (usually applied to plants) without meiosis, either by production of viable seeds without fertilisation (agamospermy) or by clonal growth of plant parts or budding of animal parts. Since meiosis is suppressed, offspring are exact genetic copies unless mutations occur (c.f. automixis).

Architomic fragmentation

A type of asexual reproduction in polychaetes in which the worm fragments into pieces each of which grows a new head and tail.

Arrhenotoky

Mode of reproduction, in which males are haploid and arise from unfertilised eggs and females are diploid and arise from fertilised eggs. This is the usual mode of reproduction in Hymenoptera.

Asexual reproduction

Production of offspring by virgin birth or by vegetative propagation.

Autogamy

1. Self-fertilisation in plants, or in hermaphrodite animals (e.g. many slugs), as opposed to out-crossing; usually referred to as selfing in animals. 2. Type of reproduction in protozoans such as Paramecium, in which the nucleus divides into two identical haploid nuclei which then fuse to form a diploid zygote.

Automixis

Asexual reproduction involving crossing over and recombination in meiosis. Diploidy is restored by fusion of the meiotic products (instead of fusion of gametes as in sexual reproduction). Because of the recombination, a parthenogenetic individual with an AB genotype can produce AA, AB and BB offspring. When automictic recombination occurs at many loci, it can give rise to a large amount of genotypic variation (c.f. apomixis).

Bisexuality

Having two sexes. In the vertebrate literature it usually refers to an organism that has both sexes present in the same individual (hermaphrodity), but in the invertebrate literature it is also used to mean gonochoristic organisms (i.e. with separate sexes).

Budding (gemmation)

A type of asexual reproduction in which a new individual is derived from an outgrowth (bud) that becomes detached from the parent. Common in Coelenterates such as Hydra, and characteristic of unicellular fungi such as yeasts.

Chiasma

The point at which paired homologous chromosomes remain in contact as they begin to separate after exchanging genetic material through crossing over during the first prophase of meiosis, forming a cross shape. The number of crossing over points is the chiasma frequency (the number of chiasmata).

Chromatin

The complex of DNA and proteins that makes up a eukaryotic chromosome.

Clone

Group of organisms that have arisen from a single individual by asexual reproduction without meiosis, and are therefore all genetically identical.

Cost of males

The immediate cost incurred by a sexual form in comparison to an otherwise identical asexual type, that it must produce males which contribute nothing to future generations except through females. Because a sexual population with a balanced sex ratio (as expected by Fisher's sex ratio theory) must invest half its growth in males, it will grow at half the rate of an otherwise identical asexual population in which all offspring are female. This prediction gives rise to the paradox of sex: sex is the prevailing mode of reproduction in the natural world, yet it seems vulnerable to invasion by asexual mutants (which do arise in nature, even amongst some vertebrates). The paradox applies only to unconfined growth, however; if resources are limited, small competitive advantages associated with the wider genotype of the sexual can be enough to cancel the two-fold growth advantage of the asexual. The paradox of sex therefore finds an ecological solution in the trade-off between competition and growth that allows species to coexist in overlapping niches.

Cost of meiosis

The cost of producing offspring that have only half of each parent's genome set. It has two components: (1) segregation load, which only occurs when heterozygotes are the favoured genotype at a particular locus; sex then results in continual production of homozygotes, whereas the heterozygote genotype can be fixed in the asexual clone. (2) Recombination load which occurs when favourable gene combinations involving alleles at several loci are broken up by meiosis; progeny may be less fit than their parents as a consequence, whereas cloned progeny have the same fitness. In general, this cost of genome dilution is relevant only at the loci determining sexual versus asexual reproduction and not at the entire genome. The cost of genome dilution reduces with inbreeding (though costs of deleterious mutations increase).

Cost of sex

Usually refers to the two-fold cost of producing males; also cost of meiosis.

Crossing over

The reciprocal exchange of portions of chromatids between homologous chromosomes during meiosis. Crossing over produces recombination by altering the patterns of genes in a chromosome.

Cryptobiosis

Dormancy, for example in cysts of the brine shrimp Artemia.

Diapause

Period of suspended development.

Dioecious

A plant species with male and female flowers on separate plants is referred to as dioecious (equivalent to gonochorism in animals).

Diploid

Having two sets of genes and two sets of chromosomes, one from the mother and one from the father.

Ephippium

Modified carapace of Daphnia which houses diapausing eggs of cyclical and obligate parthenogens. Eggs can then survive freezing and desiccation, and ephippia represent the primary dispersal stage.

Epistatic effect

The production in an organism of a character determined by genes at two or more loci, different from the characters coded individually at each locus.

Fisher's sex ratio theory

Selection acting on the individual tends to produce population sex ratios close to 1:1 even where a single male can fertilise the eggs of many females. A female-biased sex ratio, say 1M:2F, is not evolutionarily stable because an average male gets twice as many mates as each female, so a gene which causes parents to bias the sex ratio of their offspring towards males would rapidly spread. Conversely, if males are twice as common as females then daughters will be advantaged, because only one sperm fertilises each egg so only half the males can contribute genes to any individual offspring. Only when the sex ratio is exactly 1:1 will the expected success of a male and a female be equal and the population stable. When sons and daughters cost different amounts to make, the stable evolutionary strategy is for the parent to invest equally in the two sexes rather than to produce equal numbers.

Fission

A type of asexual reproduction occurring in some unicellular organisms (e.g. diatoms, protozoans, bacteria). The parent cell divides to form two (binary fission) or more similar daughter cells.

Fixation

When all members of a population are homozygous for a particular allele at a given locus, then the gene has gone to fixation (i.e. there is no polymorphism).

Frozen Niche Variation model

A model proposed by R. C. Vrijenhoek (1979) to explain the ecological coexistence of multiple asexual clones and their sexually reproducing ancestors, such as observed in topminnows and some lizards and gekkos. Multiple clones, each arising from a different sexual ancestor, are hypothesised to capture and freeze genotypic variation from the ancestors. Selection among clones then favours specialised genotypes having minimal niche overlap with established clones and the sexual ancestors. These processes generate a limited number of clones that coexist on a local scale with the sexual ancestors, as long as the cumulative niche of the clones does not eclipse the niche of the sexual ancestors.

Genetic load

Reduction in the average fitness of members of a population due to the presence of deleterious genes or combinations of genes. Can take the form of mutational, segregational, or recombinational load.

Genome

All the genes contained in a single set of chromosomes (i.e. in a haploid nucleus).

Genotype

The set of two genes at a locus possessed by an individual. More generally, the genetic composition of an organism - the particular combination of alleles it possesses.

Geographical parthenogenesis

Thelytokous forms being distributed differently from their sexual relatives. This is usually the case, but not when egg production in the thelytokous form needs to be stimulated by sperm from males (pseudo-fertilisation). Otherwise asexual forms are generally found more frequently at extreme latitudes, higher altitudes, the margins of species' ranges, on islands, and in regularly disturbed communities. Parthenogenesis facilitates colonisation of new habitat because growth rates are twice as fast as for an equivalent sexual, there is no inbreeding (loss of heterozygosity) or Allee effect.

Gonochorism

The existence of individuals of separate sexes. The normal mode of sexuality in animals is gonochoristic. Common sexual alternatives are hermaphroditism and unisexuality. Plant species with male and female flowers on separate plants are referred to as dioecious.

Gynogenesis

A form of sexuality involving strictly clonal inheritance although sperm are needed to stimulate zygote development (c.f. hybridogenesis).

Haploid

Having a single set of genes. In diploid organisms, only the gametes are haploid.

Hermaphrodite

An individual (or flower) possessing both male and female sex organs. Some are capable of self-fertilisation, others can only out-cross. Synchronous hermaphroditism is the most common form, in which both male and female states coexist functionally. Protogynous hermaphroditism occurs in some fishes, in which offspring develop first into females and turn later into males. Some fishes and molluscs (e.g. limpets Patella) show protandrous hermphriditism in which the male state differentiates first. Some invertebrates show cyclical hermaphroditism in which sexuality can oscillate. Fisher's sex ratio theory applies to hermaphrodites as to other sexual types, forcing them to commit equal resources to male and female gametes. However, they are not necessarily subject to the same two-fold cost of sex as gonochoristic species because each individual can produce offspring, provided it finds a mate. The two-fold cost only applies if an asexual mutant could be twice as fecund due to investing all its reproductive capacity in egg production, instead of half in eggs and half in sperm. There is also a cost of genome dilution (cost of meiosis), as with all types of sexual reproduction compared to asexual.

Heterogamy

Alternation between parthenogenesis and sexual reproduction.

Heterosis

Hybrid vigour (strength, disease resistance, life-span etc) displayed by the offspring from a cross between genetically different parents.

Heterozygosity

Presence of different alleles at a particular gene locus. Heterozygosity provides a measure of genetic variation, either in a population (the frequency of individuals heterozygous at a particular location) or in an individual (the proportion of gene loci that are heterozygous).

Homologous chromosomes

A pair of chromosomes having the same pattern of genes along the chromosome (although the nature of the genes may differ: see 'allele'). One member of the pair comes from the female parent and one from the male.

Homozygous

An organism is homozygous for a feature if it has two identical alleles controlling the feature (which may be both recessive or both dominant).

Hybrid

The offspring of a mating in which the parents belong to different varieties or species. Hybrid species are often sterile, but may show increased vigour (heterosis) in terms of strength, disease resistance, life-span etc. In some species, interspecific matings give rise to offspring capable of reproducing parthenogenetically.

Hybridogenesis

A form of sexuality involving the elimination at each generation of paternal chromosomes in meiosis during oogenesis. Occurs in the all-female diploid mosquito fish Poeciliopsis monarcha-lucida, which is a sexual parasite of P. lucida. All of the lucida chromosomes are lost before recombination, and the ova contain only the haploid complement of monacha chromosomes. The lucida chromosomes are acquired anew each generation by fertilisation with spermatozoa from male lucida. The monacha chromosomes, in contrast, are carried into the next generation as a clone. Thus, although paternal genes are expressed in the offspring, only the maternal genome is transmitted to the next generation.

Inbreeding depression

A loss of vigour amongst offspring occurring when closely related individuals mate, resulting from the expression of numbers of deleterious genes in a homozygous state and from a generally low level of heterozygosity. Although inbreeding can expose deleterious alleles to selection, it does not change allele frequencies but only increases the proportion of homozygotes above Hardy-Weinberg expectation.The inbreeding coefficient measures the probability of obtaining homozygosity due to a zygote obtaining copies of the same gene from parents of common ancestry.

Iteroparous

An organism that reproduces more than once in its lifetime (cf semelparous).

Karyotype

The number and structure of the chromosomes in the nucleus of a cell. All the diploid cells of an organism have identical karyotype.

Linkage disequilibrium

The statistical tendency for alleles to occur together (e.g. fair-haired individuals tend to be blue-eyed).

Locus

The place on a chromosome where a gene is located. If the gene has several alleles (i.e. takes several forms), only one of these will be present at a given locus.

Meiosis

Process of nuclear division during production of gametes in which each gamete receives only one member of a chromosome pair and genetic material can be exchanged between homologous chromosomes. The process involves replication of each chromosome of a homologous pair in a diploid cell, to give four chromatids, followed by crossing over and recombination. The first meiotic division then produces two diploid cells with shuffled gene combinations. This is followed by a second meiotic division to produce four haploid gametes.

Meiotic parthenogenesis

Several modes are possible. Commonly, the second meiotic division is abortive and the original chromosome number is then restored by fusion between second division sister nuclei (i.e. between the female pro-nucleus and the second polar body). Another mode involves pre-meiotic doubling of the chromosome number. This is rare outside the annelids, but found in the lizard Cnemidophorus uniparens and the salamander Ambystoma jeffersonianum.

Monoecious

A plant is monoecious if it has separate male and female flowers on the same individual (cf hermaphrodites whose flowers contain both male and female organs).

Mitosis

Process of nuclear division to produce two daughter nuclei, each identical to the parent, and resulting in two daughter cells with identical nuclear contents.

Mixis

The mixing of hereditary material by sexual reproduction, with progeny having different genotypes from their parents. There are two types of mixis: automixis, involving the joining of meiotic products of the same individual, and amphimixis, involving the joining of meiotic products of different individuals.

Muller's ratchet

In species with a high mutation rate, mutation-free individuals can be lost from small populations by genetic drift. If the population is haploid asexual, the loss is irreversible and mutations increase in a ratchet-like manner. No asexual individual can produce progeny with fewer mutations than it has itself. Since most mutations are deleterious, the fitness of individuals in the population deteriorates progressively. Sex can be advantageous because it can recreate mutation-free individuals. Some weaknesses of the model are: (1) it assumes haploidy, but increasing ploidy slows the process because most mutations are recessive; (2) it assumes a uniform environment, but in heterogeneous environments elimination of compound mutants may be slowed; (3) lethal mutations are eliminated in a single generation and hence do not accumulate; (4) most mutations arise in the male germ line, so male gametes may give progeny more mutations than the associated sexual recombination manages to eliminate.

Mutation

A change in the sequence of DNA base pairs resulting from substitution, addition, deletion, or rearrangement of the standard base pairs. Mutations do not damage the physical regularity of the genetic material. This means that they cause change of an allowed character into another allowed character. Mutations can only be removed from the population through their effects on fitness. In contrast, damage to DNA causes change of an allowed character into a disallowed character. As a consequence damage can be recognised by enzymes and repaired (provided a redundant copy of the template is available to replace the lost information).

Natural selection

The differential contribution of offspring to the next generation by individuals of different genetic types but belonging to the same population. In an equilibrium population, each sexually reproducing pair of individuals must produce two viable offspring before dying. In fact, females produce many more than two offspring each, and the excess fecundity contributes to Darwin's 'struggle for existence.' If natural selection acts to substitute one gene for another, it can do so by selection acting on the density dependent mortality only ('hard selection'), or by selection acting on all mortality, intrinsic as well as extrinsic ('soft selection'). Evolution proceeds at a faster rate if all mortality is selective.

Oogenesis

Production and growth of the ova (egg cells) in the animal ovary. Oogonia cells within the ovary divide mitotically to produce many oocytes. When mature, these undergo meiotic divisions to halve the number of chromosomes. The first produces a polar body and a secondary oocyte, and division of the latter produces an ovum and a second polar body.

Out-crossing

Mixing of genetic material from one individual with that from another.

Parthenocarpy

Formation of seedless fruits, which do not contribute to reproduction.

Parthenogenesis

Development of an individual from an unfertilised egg. Eggs are usually diploid (e.g. Daphnia) or triploid (e.g. Cnemidophorus lizard), so offspring are genetically identical to parents. Synonymous with agamospermy in plants, cf budding or vegetative propagation.

Phally polymorphism

The occurrence of more than one morph involving differences in male organs.

Phenotype

The observable manifestation of a specific genotype; the observable properties produced by the genotype in conjunction with its environment.

Pleiotropic

A gene which affects more than one characteristic in the phenotype. Antagonistic pleiotropisms involve a trade off, for example of high fecundity for shorter life.

Poecilogony

Having more than one developmental mode: reproductive flexibility. For example the polychaete Pygospio elegans has some populations with larvae that are brooded and others with larvae that hatch directly into the plankton. Others reproduce asexually by architomic fragmentation.

Polar body

One of two cells detached from the ovum during oogenesis.

Polymorphism

The existence of two or more genetically distinct forms contained within the same breeding population.

Polyploid

Having more than two sets of genes and chromosomes (e.g. triploid or tetraploid) in the nucleus. More common in plants than animals.

Pseudo-fertilisation

In gynogenesis, the stimulation of egg production in some thelytokous forms by male sperm, which do not however fertilise the egg and therefore do not contribute to the genotype. For example, the mosquito fish Poeciliopsis has two unisexual triploid clones P. 2monarcha-lucida and P. monarcha-2lucida. They reproduce parthenogenetically, but their zygotes (eggs) can only develop after stimulation by spermatozoides from a male of one of the sexual species. These clones are therefore sexual parasites.

Pseudogamy

Asexual reproduction initiated by pseudo-fertilisation from the sperm of a sexual form, and so without reference to the genetic material of the sperm.

Recombination

During gamete formation, the phase of meiosis in which chromosomes cross over and DNA is exchanged between the pair. Recombination shuffles the combinations of genes linked on the same chromosome. Thus genes from different chromosomes can become linked, and linked genes on the same chromosome can become unlinked, as a result of recombination. The rearrangement of genes produces offspring that have a combination of characteristics different from that of their parents. Recombination is a random process.

Red Queen model

The evolution of any ecological improvement in one species results in a deterioration in the habitat of species that interact with it, giving rise to selection for counter-adaptations in these species. Thus an individual's fitness is continually deteriorating with respect to its biotic environment, and it must continually evolve new adaptations to keep pace with the change. W. D. Hamilton has used this idea to model advantages of sexual reproduction for sexual and asexual populations that are susceptible to parasites. Parasites increase mortality and so can be strong agents of selection; they also evolve much faster than their hosts and so are quick to catch up in an evolutionary arms race. The model simulates gene matching between host and parasite and demonstrates a negative frequency dependence in which rare genes become favourable once the parasite has matched to common genes. Sexual populations gain a relative advantage over asexual populations by maintaining polymorphisms and therefore more rare genotypes. The essence of the parasite theory is that sex stores temporarily bad alleles and does not eliminate them. In this respect it contrasts to the mutation theory of Muller's ratchet, that sex facilitates the elimination of unequivocally bad alleles.

Selfing

Self-fertilisation by hermaphrodites, as opposed to out-crossing. Usually referred to as autogamy in plants.

Semelparous

An organism that produces its lifetime output of offspring in a single event over a short period (cf iteroparous).

Sexual reproduction

Production of offspring by fertilisation of an egg. In contrast to asexual reproduction, it involves meiotic recombination and out-crossing, which together create genetically diverse offspring.

Spanandry

Reduced production of males. For example, arthropod species infected with Walbachia bacteria may exhibit spanandry. In an obligate sexual such as the coffee berry borer Hypothenemus, offspring have a 1:10 ratio of males to females. Survival of the few males that are produced suggests an association with low juvenile mortality, or low variation in juvenile mortality. Fisher's sex ratio theory should apply, so skew may be non-adaptive.

Tangled Bank model

A verbal hypothesis proposed by G. Bell (1982) for the prevalence in the natural world of sex as a reproductive mode. It hypothesises that niche differentiation allows sexually reproducing types to persist in the face of invasion by asexual clones. In a heterogeneous environment, sexually generated progeny reduce competition by occupying wider niches than can be exploited by the genetically less diverse clones. The name 'Tangled Bank' derives from the last paragraph of Darwin's Origin of the Species, in which he contemplates a roadside bank with its tangle of vegetation, and the invertebrates that live amongst it and the birds that feed from them. He remarks on the variation in forms and complex inter-dependencies that permit such a diversity of life.

Thelytoky

Obligatory parthenogenesis.

Two-fold cost of sex

An anisogamous sexual population incurs an immediate cost in terms of its population growth rate, with respect to an otherwise identical asexual population, due to its requirement for males which make up half its population yet contribute nothing to future generations except through females. An asexual mutant arising out of a sexual population will have twice the growth capacity if its all-female offspring reproduce at the same rate per capita as the females among the ancestral sexual population. Fisher's sex ratio theory explains why sexual populations tend to comprise equal numbers of males and females.

Tychoparthenogenesis

Type of parthenogenesis in which females from sexually reproducing species hatch a small proportion of unfertilised eggs (typically < 10%). Both sexual and parthenogenetic reproduction co-occur within the same population. All known tychoparthenogens are automictic, reproducing via meiotic parthenogenesis. The mayfly Stenonema femoratum exhibits this breeding system.

Unisexual

Describing animals or plants with either male or female sexual organs but not both. Most advanced animals are unisexual, but plants are often hermaphrodite.

Unisexuality

Species represented only by females, where sexual reproduction normally depends upon males of other species (see hybridogenesis).

Vegetative propagation

Asexual reproduction in plants in which new individuals are produced upon separation from the parent of specialised structures such as tubers, bulbs, runners, or corms. Also applies to propagation from cuttings, and budding or architomic fragmentation in animals. Cf parthenogenesis.