Sex pheromone

Sex pheromones are pheromones released by an organism to attract an individual of the opposite sex, encourage them to mate with them, or perform some other function closely related with sexual reproduction. Sex pheromones specifically focus on indicating females for breeding, attracting the opposite sex, and conveying information on their species, age, sex and genotype after emitted by males. Volatile pheromones are characterized as sex pheromones or defensive pheromones and usually form a specific odor and are focused on alarm sensitivity.[1] Non-volatile pheromones, or cuticular contact pheromones, are more closely related to social insects as they are usually detected by direct contact with chemoreceptors on specific parts of insects (i.e. antennae, feet).

Introduction

Odours might be a kind of male "ornament" selected for by female choice; they meet the criteria Charles Darwin set out in The Descent of Man, and Selection in Relation to Sex. After many years of study the importance of chemical communication in this area is becoming clear.[2]

Ciliate protozoan

Blepharisma japonicum is a ciliate protozoan that displays nuclear dimorphism, having a diploid micronucleus and a polyploid macronucleus. B. japonicum produces sexual pheromones that promote conjugation.[3][4] There are two mating types (I and II), each type excreting a specific pheromone (termed gamone 1 and gamone 2, respectively). When sexually mature mating-type I cells are moderately starved, they autonomously produce and secrete gamone I.[3] Gamone 1 specifically acts on mating-type II cells, transforming them so that they can unite with type I cells, and inducing them to secrete gamone 2. Gamone 2 then transforms type I cells so that they can unite with type II cells. Cells that can unite may then undergo conjugation.

Green algae

Volvox is a genus of chlorophytes, a type of green algae. Different species form spherical colonies of up to 50,000 cells. One well-studied species, Volvox carteri (2,000 – 6,000 cells) occupies temporary pools of water that tend to dry out in the heat of late summer. As their environment dries out, asexual V. carteri quickly die. However, they are able to escape death by switching, shortly before drying is complete, to the sexual phase of their life cycle that leads to production of dormant desiccation-resistant zygotes. Sexual development is initiated by a glycoprotein pheromone.[5] This pheromone is one of the most potent known biological effector molecules. It can trigger sexual development at concentrations as low as 10−16 M.[5] Kirk and Kirk showed that sex-inducing pheromone production can be triggered experimentally in somatic cells by heat shock.[6] Thus heat shock may be a condition that ordinarily triggers sex-inducing pheromone in nature.[5]

The Closterium peracerosum-strigosum-littorale (C. psl) complex is a unicellular, isogamous charophycean alga group that is the closest unicellular relative to land plants. Heterothallic strains have two mating types, mt(-) and mt(+). When cells of opposite mating types are mixed in a nitrogen-deficient mating medium, mt(-) and mt(+) cells pair with each other and release protoplasts. This release is then followed by protoplast fusion (conjugation) leading to formation of a diploid zygospore. Sex pheromones termed protoplast-release inducing proteins (glycopolypeptides) produced by mt(-) and mt(+) cells facilitate this process.[7]

Fungi

Among fungi, pheromones promote sexual interaction in numerous species including the aquatic fungus Allomyces macrogynus, the Mucorales fungus Mucor mucedo, Neurospora crassa and the yeasts Saccharomyces cerevisiae, Schizosaccharomyces pombe and Rhodosporidium toruloides.[8][9][10] These fungi use a variety of different molecules in their sexual communication, including small molecules, such as steroids, other lipids, peptides, and derivatives of organic acid, as well as large molecules, such as glycoproteins. Although sex pheromones are ordinarily transmitted through an aqueous medium, they may also be transmitted through the air as occurs in the fungus Mucor mucedo.[11]

Sexual communication and the sexual life cycle have been especially well detailed in S. cerevisiae and S. pombe. In these yeasts mating occurs between two cells of opposite mating type and is controlled by the reciprocal action of pheromones. Cells of each mating type release pheromones that induce mating through promotion of alterations in cells of the opposite mating type. The two cells then conjugate to form a diploid zygote that may undergo meiosis. Meiosis leads to sporulation and release of ascospores that may germinate to form haploid cells, thus completing the sexual cycle. The pheromones produced by these yeasts have been identified as short peptides.[10][12]

Moths

Sex pheromones are an important factor in finding a mating partner. When a female releases chemicals, the mate search is initiated, and the male moths begin their upwind motion toward their potential partner. Sex pheromones in particular are associated with long-range chemical communication of sex substances used in signaling a mating partner.[1] Mate finding in moths involve sex pheromones that have the ability to propel long-distances and are emitted by the females abdominal glands in most cases.[13] Responsiveness to sounds or behaviors due to pre-exposure to pheromones is common within the moth species. Studies have shown that when sex pheromones are present, male moths have a decreased level of response to predation sounds versus pheromonal cues as seen in Spodoptera littoralis.[14] An increased responsiveness in the antennal lobe when pre-exposed to the sex pheromones shown in studies is considered a long-term effect exhibited post twenty-four hours and serves as an advantage for males where they can alter their performance in advance prior to encountering a female that is reproductively active [15] However, this is also a disadvantage where the moth’s fitness decreases since they require more maintenance associated with their long-term memory neural structures.[15]

Butterflies

Chemoreception of sexual odorants by male insects has been considered to be very effective and sharp.[1] The Bicyclus anynana species is known for their close-range pheromone response as opposed to the moths’ long-range pheromonal response.[16] As for the male butterfly of the subfamily Lycorea, they have a pair of brush like structures on their abdomens named “hair pencils” that produce odors. The odors are given off in their aerial path while trying to find a mate.[1] After finding a potential mate, the male induces the female by brushing the “hair pencils” against her antennae later leading to copulation.[1] Males release close-range pheromones from their hair pencils and folds on their wings.[16]

The androconia gland in butterflies is responsible for emission of scents from pheromones produced during the wing fluttering during courtship when attracting a female (Costanzo & Monteiro, 2007). In the colias species of butterflies, the glands are found on the wing and are released during the ‘wing clapping’ stage of courtship.[17] Males secreting the pheromonal cues not only have glands on their antennae but some Bicyclus species have patches of velvety scales located on the dorsal surface of their forewing where pheromones are released.[16] The released pheromones are received by olfactory receptors on the antennae.

The Pieris napi butterfly uses the release of citral as a male sex pheromone signal produced by males directed to females during courtship.[18] Most of the chemical cues produced by males are associated to a female response involving courtship, mate-choice, species-specific identification and sex-specific signals.[18] The scents are also said to influence male-male competition and forcing males to guard their mating territories. The citral pheromone is also released during male-male competition as pheromones are released during most male flight activity however; there is a less of a response to males as when compared to females. Females have higher antennae sensitivity to the citral pheromones rather than males, triggering a reduced reaction by males.[18]

Fruit flies

Drosophila melanogaster males are known for their elaborate courtship rituals, where they follow a female, tap on her with his forelegs and “sing” a courtship song through rapid wing clapping sounding much like a vibration sound in an attempt to entice her.[19] He then proceeds to contact her genitalia with his mouth and curve his abdomen to induce copulation.[19] During the early stages of courtship where the male taps the female with his forelegs, males are able to sense the gender and species type of a potential female through the use of non-volatile (i.e. cuticular) pheromones and gustatory receptor neurons (GRNs) located on the males forelegs. This process is known as gustation where non-volatile pheromones are detected by the GRNs and processed later inducing courtship.[19]

Drosophila flies exhibit specific relationships between neurons and behavior. Much of the courtship activity involved in the sexual mating process for this species of flies involves mapping neuronal circuitry. As for the neuronal content of the olfactory cues, in both vertebrates and insects, olfactory sensory neurons (OSNs) extend from the dendrites that are responsible for interacting with odors from the environment and are then recognized by distinct odorant receptor (OR) proteins that are located in the dendritic membrane.[20] Since there are two distinct forms of anatomical connections in the olfactory interneurons of the third order olfactory interneurons of the lateral horn of the drosophila melanogaster, these neurons may be the first elements in the olfactory pathway that respond to sex-specific stimuli.[19] Therefore it is certain that there is a relationship between pheromones, olfaction and courtship.

Wasps

Parasitic wasps are carnivorous insects that feed on other insects. Behavioral studies have shown that males influence females reproductive behavior through chemical signaling, increasing the male’s reproductive success.[21] During ejaculation, males release pheromones along with sperm which induce psychological and behavioral changes in females such as rejection of courting males.[21] The behavioral changes induced during the first copulation later enables the male to father numerous offspring of the same female.[21]

Much insect behavior involves a high male-male competition for a receptive female and the male is usually responsible for releasing sex pheromones in an attempt to attract a female. During male-male competition when racing to a female, the release of pheromone serves as an indication to the male of genetic quality where males are more attracted to a female that releases a large amount of pheromones to attract them.[21]

Earthworms

Earthworms are hermaphrodites, that is, they have both male and female sexual organs. Although most earthworm matings occur between two different individuals (outcrossing) some earthworm lineages are mostly parthenogenetic. In Hormogaster samnitica and Hormogaster elisae transcriptomes, DNA libraries were sequenced and two pheromones, Attractin and Temptin, were detected in all tissue samples of both species.[22] These pheromones likely act as attractants that promote outcrossing.

Mealworm beetle

A sex pheromone released by male Tenebrio molitor has been identified[23] T. molitor females are more attracted to pheromonal odors of outbred males than of inbred males.[24] This suggests that inbreeding reduces the attractiveness of male sexual signaling.

Sea hare

Aplysia is a genus of sea hares that is a clade of large sea slugs, marine gastropod mollusks. Aplysia californica is a simultaneous hermaphrodite so that adult organisms have both male and female sexual organs at the same time. Potent water-borne phermones are employed in promoting and maintaining mating between different individuals.[25]

Moss

In non-vascular plants, sexual reproduction depends on unicellular free-motile sperm traveling from male to female reproductive structures across the terrestrial landscape. Recent evidence suggests that microarthropods (e.g. springtails and oribatid mites) can disperse sperm in mosses. Tissues of the moss Ceratodon purpureus emit complex volatile scents, similar in diversity to those in pollination mutualisms between flowering plants and insects.[26] The chemical composition of C. purpureus volatiles are sex-specific, and moss dwelling microarthropods are differentially attracted to these sex-specific moss volatile cues. These findings indicate the emergence of a scent-based “plant-pollinator-like” relationship between two of Earth’s most ancient terrestrial lineages, mosses and microarthropods.

Birds

A chemical communication in vertebrates is not as important as visual and auditory communication and is widely understudied for many species such as birds. For the spotless starling Sturnus unicolor, a study has shown that the starling is able to discriminate the sex within their species using olfactory cues. The hormones secreted by the uropygial gland convey information on sex, age and reproductive status.[27] The uropygial gland is an opening located on most avian species towards the base of the tail. The gland secretes an oily fluid associated with preening, or cleaning of the feathers. The uropygial gland itself is said to be associated with the secretion of specific chemical cues enabling the functioning of the gland as a chemical signal used in mate choice.[27]

Chemical cues are not the only factor when it comes to secretions by the uropygial gland. The sex, age and reproductive status are all factors as the sex is important as males are usually searching for females and vice versa for females; however, they are all attracted to male scents in some way. Age is an important factor as birds with 12-14 day old nestlings are almost fully feathered causing lower levels of the main component in adults (hexadecanol) and greater proportions of methyl ketones compared with adults. This could be accredited to differences in diet or differences in the availability of resources.[27] During the breeding period, adults release an increased level of pheromones also since their uropygial glands are larger while raising their nestlings.[27] Intrasexual aggression is exhibited when males respond to other males pheromones released by the uropygial gland in order to mark their social dominance and their competitor territories.[27] Intrasexual competition accounts for the preference by males for other male scents. Most of the blends of excretions are species-specific therefore many avian species are aware of their own species secretions making them less receptive to the cues released.

Amphibians

Frogs and salamanders behave similarly through the use of chemical communication as a source of survival (Waldman, 2004). For example, the tree frog Litoria splendida secretes several biologically active peptides (Rajchard, 2005). An aquatic female usually attracts pheromones secreted by the parotid and rostral glands of this particular frog species (Rajchard, 2005). There was no discrimination found between frogs and their own odor along with their surroundings within their home range (Waldman, 2004). As in many animals, frogs adapt to their environment and can sense several odors surrounding them. Frogs remain under rocks and secluded during daylight hours and emerge at night therefore they highly rely on chemical signals to assess their surroundings prior to emerging (Waldman, 2004). By sensing chemical signals such as pheromones, frogs can become aware of potential competitors nearby. Chemosignals serve as a basis of communication to enhance the fitness of the signalers, which serves as an ultimate cause for the frogs daily activity and reactions to their environment (Waldman, 2004).

Salamanders also exhibit sexual roles of pheromones and their interactions with hormones where males of salamanders of the Plethodontidae family deliver pheromones through their chin gland in order to increase the female receptivity and mate choice (Rajchard, 2005). This pheromonal activity is said to be just as effective as the conspecific pheromones associated with moths and their receptivity to the pheromones released. Not only is female receptivity increased but male courtship success is also increased as in terrestrial salamanders where the pheromones are received by the accessory olfactory system, known for detecting pheromones (Rajchard, 2005). Salamanders can also distinguish between chemical cues of their own and of their surroundings therefore they are able to differentiate between mates and creatures within their environment (Waldman, 2004).

Lizards and snakes

The chemoreception system is heavily used by lizard and snake species because they produce chemical secretions that are often deposited in urine, feces or substrate scents in order to attract mates (Martín & López, 2012). The chemicals in the scent or trailing marks of lizards and snakes may give information on sex, body size, or age, which can then be used by females to detect areas that are scent marked by preferred potential males (Martín & López, 2012). Many snakes, just as many bird species, rely on their chemosensory abilities to detect mates (Shine & Mason, 2012). Scents are detected in two ways, through olfaction or airborne cues through the nostril or vomerolfaction where substrates are accessed through the forked tongue and vomeronasal system (Mason & Parker, 2010). The vomeronasal system is the driving force in sexual behavior of snakes and olfaction is used to develop underlying information about their prey (Shine & Mason, 2012). Chemical cues of snakes are often incapable of diffusing through air as they are large epidermal lipids therefore they must use tongue-flicking techniques to determine characteristics of potential mates (Shine & Mason, 2012). In both, lizards and snakes, substrate-borne cues are preferred over airborne cues however, if molecules are small enough to diffuse through air, then olfaction is preferred (Shine & Mason, 2012).

Male lizards have a way of “luring” females to their territories through food scent marks as many females are usually interested in the quality of the territory that the male defends rather that the male himself (Martín & López, 2012). This increases male-male competition for territories where males want to occupy favorable areas with many food sources and resources in order to attract females (Martín & López, 2012). Lizards usually use scent marks to determine the quality of the male occupying the territory (i.e. fitness, health, immune response) or the presence of food and resources, meaning the territory is of high quality (Martín & López, 2012). The Carpetan rock lizard, Iberolacerta cyreni, is a polygynandrous species that is known for their discrimination of scent marks based on age (Martín & López, 2013). Studies have shown that females were more attracted to pheromones produced by older males as they are able to produce more pheromones than younger males and females also preferred areas occupied by many males rather than one where there is a higher level of signal (Martín & López, 2013).

In other lizard species, such as the P. hispanicus, body coloration is used along with odor cues (López et al., 2002). Males are often sexual dichromatic, where one sex displays brighter colors than females on their belly (López et al., 2002). Over all, it was seen that most lizards prefer odor cues over color patterns when choosing a mate (López et al., 2002). Tongue-flick explorations are usually followed by reception of chemical cues to confirm a suitable female is in close-range since olfactory cues are more favorable when in close-range rather than color cues, which are preferred in long-range mating (López et al., 2002).

Spiders

Two types of pheromones emitted by spiders include contact and airborne pheromones. Airborne pheromones are for long-range use and are not successful in determining a female’s location due to aggregation (Gaskett, 2007). Contact pheromones provide specific information on female’s location and qualities which is vital for cannibalistic species allowing a potential mate assess and reject a female prior to entering her web for mating (Gaskett, 2007). Males have chemoreceptors located on their pedipalps and forelegs that are able to detect the strong pheromones emitted by females. The female desert spider, Agenelopsis aperta, is part of the Agenelidae family which use volatile pheromones to attract males (Schulz, 2013). The common spider family, Linyphiidae, is well known for their silk-rich webs. Pheromones are largely produced during web production in large amounts therefore when a male enters the web to begin mating; they cut away the threads of the web and roll them up. The ultimate cause of this behavior is to reduce the evaporation of the attracting pheromone and decrease the chances of interruption by a competing male since courtship is a timely process (Schulz, 2013).

In most cases of spider mating, sex pheromones are emitted by the female and received by the male. Female spiders directly release sex pheromones from their body cuticle or web silk. An advantage of not emitting volatile pheromones from a gland allows for spiders to catch prey and attract mating partners (Gaskett, 2007). Male spiders are often choosy and prefer virgin females (Gaskett, 2007). The first mating with a female is important as possible future concerns include: sperm priority and future males may be disinterested in a female that is not a virgin (Gaskett, 2007).

Mice

Mice can distinguish close relatives from more distantly related individuals on the basis of scent signals.[28] This allows mice to avoid mating with close relatives and to minimize inbreeding. Jimenez et al.[29] showed that the inbreeding of mice derived from wild populations significantly reduced survival when such mice were reintroduced into a natural habitat.

Mate choice and sexual selection

Females of the tiger moth Utetheisa ornatrix choose males that produce more pheromones.

Males usually compete for scarce females, which make adaptive choices based on male traits. The choice can benefit the female directly and/or genetically. An example is female tiger moths (Utetheisa ornatrix) choosing males that produce the most pheromone; an honest signal of the amount of protective alkaloids the male has, as well as an indicator of the size of female offspring (females fertilised by such males lay more eggs).[2] Male cockroaches form dominance hierarchies based on pheromone "badges", while females use the same pheromone for male choice.[30]

In most species the non-limiting sex calls. Some female moths signal, but this is cheap/low risk; it means the male has to fly to her (high risk). This mirrors communication with other sensory modalities, e.g. male frogs croak; male birds are usually colourful. Male long-range pheromone signals may be associated with patchy resources for the female. In some species both sexes signal. Males can sometimes attract other males instead, the sex pheromone acting as an aggregation pheromone.[2]

External fertilization and chemical duets

It is likely that most externally fertilizing species (e.g. marine worms, sea urchins) coordinate their sexual behaviour (release of sperm and eggs) using pheromones. This coordination is very important because sperm are diluted easily, and also die after a short amount of time.[2]

The main selective advantage of outcrossing compared to inbreeding appears to be that outcrossing promotes the masking of deleterious recessive alleles, while inbreeding promotes their harmful expression.[31][32]

Discussion

Sex pheromones have evolved in many species. The many types of pheromones (i.e. alarm, aggregation, defense, sexual attraction) all have a common cause acting as chemical cues to trigger a response. However, sex pheromones are particularly associated with signaling mating behaviors or dominance. The odors released can be seen as a favorable trait selected by either the male or female leading to attraction and copulation. Chemical signaling can even be used to find genetically different mates and avoid inbreeding.[33] Females are often choosy when deciding to mate with a male and chemical communication ensures that they find a high-quality mate that satisfies their reproduction needs.

Additional reading

References

  1. ↑ 1.0 1.1 1.2 1.3 1.4 (Regnier & Law, 1968)
  2. ↑ 2.0 2.1 2.2 2.3 Wyatt, T. (2003) Pheromones and Animal Behaviour. Cambridge University Press
  3. ↑ 3.0 3.1 Miyake, A. (1981). Cell interaction by gamones in Blepharisma In: Sexual Interactions in Eukaryotic Microbes (O’Day, D.H. & Horgen, F.A., eds), pp. 95-129 New York: Academic Press.
  4. ↑ Sugiura M, Shiotani H, Suzaki T, Harumoto T (2010). "Behavioural changes induced by the conjugation-inducing pheromones, gamone 1 and 2, in the ciliate Blepharisma japonicum". Eur. J. Protistol. 46 (2): 143–9. doi:10.1016/j.ejop.2010.01.002. PMID 20167456.
  5. ↑ 5.0 5.1 5.2 Hallmann A, Godl K, Wenzl S, Sumper M (1998). "The highly efficient sex-inducing pheromone system of Volvox". Trends Microbiol. 6 (5): 185–9. PMID 9614342.
  6. ↑ Kirk DL, Kirk MM (1986). "Heat shock elicits production of sexual inducer in Volvox". Science 231 (4733): 51–4. PMID 3941891.
  7. ↑ Sekimoto H, Satoh S, Fujii T (1990). "Biochemical and physiological properties of a protein inducing protoplast release during conjugation in theClosterium peracerosum-strigosum-littorale complex". Planta 182 (3): 348–54. doi:10.1007/BF02411384. PMID 24197184.
  8. ↑ O’Day, D.H. (1981) Modes of cellular communication and sexual interactions in eukaryotic microbes. In: Sexual Interactions in Eukaryotic Microbes. (O’Day, D.H. & Horgen, P.A. eds pp. 3-17. New York; Academic Press.
  9. ↑ Akada R, Minomi K, Kai J, Yamashita I, Miyakawa T, Fukui S (1989). "Multiple genes coding for precursors of rhodotorucine A, a farnesyl peptide mating pheromone of the basidiomycetous yeast Rhodosporidium toruloides". Mol. Cell. Biol. 9 (8): 3491–8. PMC 362396. PMID 2571924.
  10. ↑ 10.0 10.1 Davey J (1992). "Mating pheromones of the fission yeast Schizosaccharomyces pombe: purification and structural characterization of M-factor and isolation and analysis of two genes encoding the pheromone". EMBO J. 11 (3): 951–60. PMC 556536. PMID 1547790.
  11. ↑ Jones, B.E., Williamson, I.P. & Gooday, G.W. (1981). Sex pheromones in Mucor. In: Sexual Interactions in Eukaryotic Microbes (O’Day, D. H. & Horgen, P.A.,eds), pp. 179-198. New York: Academic Press.
  12. ↑ Manney T.R., Buntze, W., & Betz R. (1981). The isolation, characterization and physiological effects of the Saccharomyces cerevisiae sex pheromones. In: Sexual Interactions in Eukaryotic Microbes (O’Day, D. H. & Horgen, P.A.,eds), pp. 21 - 51. New York: Academic Press.
  13. ↑ (Roelofs et al., 2002)
  14. ↑ (Skals et al., 2005)
  15. ↑ 15.0 15.1 (Anderson et al., 2007)
  16. ↑ 16.0 16.1 16.2 (Costanzo & Monteiro, 2007)
  17. ↑ (Rutowski, Dickinson, & Terkanian, 1991)
  18. ↑ 18.0 18.1 18.2 (Andersson et al., 2007)
  19. ↑ 19.0 19.1 19.2 19.3 (Pavlou & Goodwin, 2013)
  20. ↑ (Keller & Vosshall, 2003)
  21. ↑ 21.0 21.1 21.2 21.3 (Ruther et al., 2007)
  22. ↑ Novo M, Riesgo A, Fernández-Guerra A, Giribet G (2013). "Pheromone evolution, reproductive genes, and comparative transcriptomics in mediterranean earthworms (annelida, oligochaeta, hormogastridae)". Mol. Biol. Evol. 30 (7): 1614–29. doi:10.1093/molbev/mst074. PMID 23596327.
  23. ↑ Bryning GP, Chambers J, Wakefield ME (2005). "Identification of a sex pheromone from male yellow mealworm beetles, Tenebrio molitor". J. Chem. Ecol. 31 (11): 2721–30. doi:10.1007/s10886-005-7622-x. PMID 16273437.
  24. ↑ Pölkki M, Krams I, Kangassalo K, Rantala MJ (2012). "Inbreeding affects sexual signalling in males but not females of Tenebrio molitor". Biol. Lett. 8 (3): 423–5. doi:10.1098/rsbl.2011.1135. PMC 3367757. PMID 22237501.
  25. ↑ Cummins SF, Nichols AE, Schein CH, Nagle GT (2006). "Newly identified water-borne protein pheromones interact with attractin to stimulate mate attraction in Aplysia". Peptides 27 (3): 597–606. doi:10.1016/j.peptides.2005.08.026. PMID 16309784.
  26. ↑ Rosenstiel TN, Shortlidge EE, Melnychenko AN, Pankow JF, Eppley SM (2012). "Sex-specific volatile compounds influence microarthropod-mediated fertilization of moss". Nature 489 (7416): 431–3. doi:10.1038/nature11330. PMID 22810584.
  27. ↑ 27.0 27.1 27.2 27.3 27.4 (Amo et al., 2012)
  28. ↑ Sherborne AL, Thom MD, Paterson S, Jury F, Ollier WE, Stockley P et al. (2007). "The genetic basis of inbreeding avoidance in house mice". Curr. Biol. 17 (23): 2061–6. doi:10.1016/j.cub.2007.10.041. PMC 2148465. PMID 17997307.
  29. ↑ Jiménez JA, Hughes KA, Alaks G, Graham L, Lacy RC (1994). "An experimental study of inbreeding depression in a natural habitat". Science 266 (5183): 271–3. PMID 7939661.
  30. ↑ Moore, A. J., & Moore, P. J. (1999). Balancing sexual selection through opposing mate choice and male competition. Proceedings of the Royal Society of London. Series B: Biological Sciences, 266(1420), 711-716. doi: 10.1098/rspb.1999.0694
  31. ↑ Bernstein H, Hopf FA, Michod RE. (1987). The molecular basis of the evolution of sex. Adv Genet 24:323-70. Review. PMID 3324702
  32. ↑ Michod, R.E. (1994). “Eros and Evolution: A Natural Philosophy of Sex” Addison-Wesley Publishing Company, Reading, Massachusetts. ISBN 0201442329 ISBN 978-0201442328
  33. ↑ Bernstein C, Bernstein H (1997). "Sexual communication". J. Theor. Biol. 188 (1): 69–78. doi:10.1006/jtbi.1997.0459. PMID 9299310.