Sexual dimorphism

Female (left) and male (right) common pheasant, illustrating the dramatic difference in both color and size between sexes

Sexual dimorphism is a phenotypic differentiation between males and females of the same species. The prototypical example is for differences in characteristics of reproductive organs. Other possible examples are for secondary sex characteristics, body size, physical strength and morphology, ornamentation, behavior and other bodily traits. Traits such as ornamentation and breeding behavior found in one sex only imply sexual selection.

Examples

The peacock, on the right, is courting the peahen, on the left.
Male (bottom) and female mallards. The male mallard has an unmistakable green head.
Female (left) and Male (right) Argiope appensa, displaying typical sexual dimorphism differences in spiders where the male is dramatically smaller.
Orgyia antiqua male and female.

Ornamentation and coloration

A common type of dimorphism is ornamentation. A frequent component of such dimorphic ornamentation is sexual dichromatism, meaning that the sexes of a given species differ in coloration, such as is conspicuously the case in many species of birds and reptiles.[1][2]

Exaggerated dimorphic traits are used predominantly in the competition over mates, implying sexual selection.[3] Ornaments may be costly to produce or maintain, which has complex evolutionary implications[4] but the costs and implications differ depending on the nature of the ornamentation (such as the colour mechanism involved).

The peafowl constitute conspicuous illustrations of the principle. The ornate plumage of peacocks, as used in the courting display, attracts peahens. At first sight one might mistake peacocks and peahens for completely different species because of the vibrant colours and the sheer size of the male's plumage; the peahen being of a subdued brown coloration. The plumage of the peacock increases its vulnerability to predators because it is a hindrance in flight, and it renders the bird conspicuous in general. Similar examples are manifold, such as in Birds of Paradise and Argus pheasants.

Another example of sexual dichromatism is that of the nestling blue tits. Males are chromatically more yellow than females. It is believed that this is obtained by the ingestion of green lepidopteran larvae, which contain large amounts of the carotenoids lutein and zeaxanthin.[5] This diet also affects the sexually dimorphic colours in the human-invisible UV spectrum.[6][7] Hence, the male birds, although appearing yellow to humans actually have a violet-tinted plumage that is seen by females. This plumage is thought to be an indicator of male parental abilities.[8] Perhaps this is a good indicator for females because it shows that they are good at obtaining a food supply from which the carotenoid is obtained. There is a positive correlation between the chromas of the tail and breast feathers and body condition.[1] Carotenoids play an important role in immune function for many animals, so carotenoid dependent signals might indicate health.[9]

In many instances, females show preference for exaggerated male secondary sexual characteristics when choosing a mate.[10] Females tend to show direction preferences for more elaborate males.[3] Females have been shown to discriminate against males which are dull in color regardless of the species' vision.[11] There have also been species such as estrildid finch where premating isolation was seen due to lack of vibrant colors by the males. This female preference for ornamentation may affect the evolution of discriminatory mating preferences.[11] This is known as the ornamentation hypothesis.

Similar sexual dimorphism and mating choice are also observed in many fish species. For example, in guppies males have colorful spots and ornamentations while females are generally grey in color. Female guppies prefer brightly colored males to duller males.

Psychological and behavioral differentiation

Sex steroid-induced differentiation of adult reproductive and other behavior has been demonstrated experimentally in many animals. In some mammals, adult sex-dimorphic reproductive behavior (e.g., mounting or receptive lordosis) can be shifted to that of the other sex by supplementation or deprivation of androgens in fetal life or early infancy, even if adult levels are normal.

Physiological differentiation

In redlip blennies, only the male fish develops an organ at the anal-urogenital region that produces antimicrobial substances. During parental care, males rub their anal-urogenital regions over their nests' internal surfaces, thereby protecting their eggs from microbial infections, one of the most common causes for mortality in young fish.[12]

Evolution

In 1871 Charles Darwin advanced the theory of sexual selection, which related sexual dimorphism with sexual selection.

It has been proposed that the earliest sexual dimorphism is the size differentiation of sperm and eggs (anisogamy), but the evolutionary significance of sexual dimorphism is more complex than that would suggest.[13] Anisogamy and the usually large number of small male gametes relative to the larger female gametes usually lies in the development of strong sperm competition,[14][15] because small sperm enable organisms to produce a large number of sperm, and make males (or male function of hermaphrodites[16]) more redundant. This intensifies male competition for mates, and promotes the evolution of other sexual dimorphim in many species, especially in vertebrates, including mammals. However, in some species, the females can be larger than males, irrespective of gametes, and in some species females (usually of species in which males invest a lot in rearing offspring and thus no longer considered as so redundant) compete for mates in ways more usually associated with males.

In many non-monogamous species, the benefit to a male's reproductive fitness of mating with multiple females is large, whereas the benefit to a female's reproductive fitness of mating with multiple males is small or nonexistent.[17] In these species, there is a selection pressure for whatever traits enable a male to have more matings. The male may therefore come to have different traits from the female.

Male (left), offspring, and female (right) Sumatran orangutans.

These traits could be ones that allow him to fight off other males for control of territory or a harem, such as large size or weapons;[18] or they could be traits that females, for whatever reason, prefer in mates.[19] Male-male competition poses no deep theoretical questions[20] but mate choice does.

Females may choose males that appear strong and healthy, thus likely to possess "good alleles" and give rise to healthy offspring.[21] However, in some species females seem to choose males with traits that do not improve offspring survival rates, and even traits that reduce it (potentially leading to traits like the peacock's tail).[20] Two hypotheses for explaining this fact are the sexy son hypothesis and the handicap principle.

The sexy son hypothesis states that females may initially choose a trait because it improves the survival of their young, but once this preference has become widespread, females must continue to choose the trait, even if it becomes harmful. Those that do not will have sons that are unattractive to most females (since the preference is widespread) and so receive few matings.[22]

The handicap principle states that a male who survives despite possessing some sort of handicap thus proves that the rest of his genes are "good alleles". If males with "bad alleles" could not survive the handicap, females may evolve to choose males with this sort of handicap; the trait is acting as a hard-to-fake signal of fitness.[23]

Species with females larger than males

In some species, such as many insects, many spiders, many fish, many reptiles, birds of prey and certain mammals such as the spotted hyena, and blue whale, the female is larger than the male. As an example, in some species, females are sedentary and sparsely distributed, and so males must search for them. Fritz Vollrath and Geoff Parker argue that this difference in behaviour leads to radically different selection pressures on the two sexes, evidently favouring smaller males.[24] Cases where the male is larger than the female have been studied as well,[24] and require alternative explanations.

One example of sexual size dimorphism is the bat Myotis nigricans, where females are substantially larger than males in terms of body weight, skull measurement, and forearm length.[25] The interaction between the sexes and the energy needed to produce viable offspring make it favorable for females to be larger in this species. Females bear the energetic cost of producing eggs, which is much greater than the cost of making sperm by the males. The fecundity advantage hypothesis states that a larger female is able to produce more offspring and give them more favorable conditions to ensure their survival; this is true for most ectotherms. A larger female can provide parental care for a longer time while the offspring matures. The gestation and lactation periods are fairly long in M. nigricans, the females suckling their offspring until they reach nearly adult size.[26] They would not be able to fly and catch prey if they did not compensate for the additional mass of the offspring during this time. Smaller male size may be an adaptation to increase maneuverability and agility, allowing males to compete better with females for food and other resources.

Female triplewart seadevil, an anglerfish, with male attached near vent (arrow)

Some species of anglerfish also display extreme sexual dimorphism. Females are more typical in appearance to other fish, whereas the males are tiny rudimentary creatures with stunted digestive systems. A male must find a female and fuse with her: he then lives parasitically, becoming little more than a sperm-producing body. A similar situation is found in the Zeus water bug Phoreticovelia disparata where the female has a glandular area on her back that can serve to feed a male, which clings to her (note that although males can survive away from females, they generally are not free-living).[27]

Some plant species also exhibit dimorphism in which the females are significantly larger than the males, such as in the moss Dicranum[28] and the liverwort Sphaerocarpos.[29] There is some evidence that, in these genera, the dimorphism may be tied to a sex chromosome,[29][30] or to chemical signalling from females.[31]

Another complicated example of sexual dimorphism is in the Vespula squamosa, or southern Yellowjacket. In this wasp species, the female workers are the smallest, the male workers are slightly larger, and the female queens are significantly larger than her female worker and male counterparts.

Plants

Most plants are hermaphroditic but approximately 6% have separate males and females (dioecy).[32] Males and females in insect-pollinated species generally look similar to one another because plants provide rewards (e.g. nectar) that encourage pollinators to visit another similar flower, completing pollination. Catasetum orchids are one interesting exception to this rule. Male Catasetum orchids violently attach pollinia to euglossine bee pollinators. The bees will then avoid other male flowers but may visit the female, which looks different from the males.[33]

Various other dioecious exceptions, such as Loxostylis alata have visibly different genders, with the effect of eliciting the most efficient behaviour from pollinators, who then use the most efficient strategy in visiting each gender of flower instead of searching say, for pollen in a nectar-bearing female flower.

Some plants, such as some species of Geranium have what amounts to serial sexual dimorphism. The flowers of such species might for example present their anthers on opening, then shed the exhausted anthers after a day or two and perhaps change their colours as well while the pistil matures; specialist pollinators are very much inclined to concentrate on the exact appearance of the flowers they serve, which saves their time and effort and serves the interests of the plant accordingly. Some such plants go even further and change their appearance again once they have been fertilised, thereby discouraging further visits from pollinators. This is advantageous to both parties because it avoids damage to the developing fruit and avoids wasting the pollinator's effort on unrewarding visits. In effect the strategy ensures that the pollinators can expect a reward every time they visit an appropriately advertising flower.

Females of the aquatic plant Vallisneria americana have floating flowers attached by a long flower stalk that are fertilized if they contact one of the thousands of free floating flowers released by a male.[34] Sexual dimorphism is most often associated with wind-pollination in plants due to selection for efficient pollen dispersal in males vs pollen capture in females, e.g. Leucadendron rubrum.[35]

Sexual dimorphism in plants can also dependent on reproductive development. This can be seen in Cannabis sativa, a type of hemp, which have higher photosynthesis rates in males while growing but higher rates in females once the plants become sexually mature.[36]

It also should be borne in mind that every sexually reproducing extant species of vascular plant actually has an alternation of generations; the plants we see about us generally are diploid sporophytes, but their offspring really are not the seeds that people commonly recognise as the new generation. The seed actually is the offspring of the haploid generation of microgametophytes (pollen) and megagametophytes (the embryo sacs in the ovules). Each pollen grain accordingly may be seen as a male plant in its own right; it produces a sperm cell and is dramatically different from the female plant, the megagametophyte that produces the female gamete.

Fish

There are also cases where males are substantially larger than that of females. An example is Lamprologus callipterus, a type of cichlid fish. In this fish, the males are characterized as being up to 60 times larger than that of the females. The male's increased size is believed to be advantageous because males collect and defend empty snail shells in each of which a female breeds.[37] Males must be larger and more powerful in order to collect the largest shells. The female's body size must remain small because in order for her to breed, she must lay her eggs inside the empty shells. If she grows too large, she will not fit in the shells and will be unable to breed. Another example is the dragonet, in which males are considerably larger than females and possess longer fins.

The female's small body size is also likely beneficial to her chances of finding an unoccupied shell. Larger shells, although preferred by females, are often limited in availability.[38] Hence, the female is limited to the growth of the size of the shell and may actually change her growth rate according to shell size availability.[39] In other words, the male's ability to collect large shells depends on his size. The larger the male, the larger the shells he is able to collect. This then allows for females to be larger in his brooding nest which makes the difference between the sizes of the sexes less substantial. Male-male competition in this fish species also selects for large size in males. There is aggressive competition by males over territory and access to larger shells. Large males win fights and steal shells from competitors. Sexual dimorphism also occurs in hermaphroditic fish. These species are known as sequential hermaphrodites. In fish, reproductive histories often include the sex-change from female to male where there is a strong connection between growth, the sex of an individual, and the mating system it operates within.[40] In protogynous mating systems where males dominate mating with many females, size plays a significant role in male reproductive success.[41] Males have a propensity to be larger than females of a comparable age but it is unclear whether the size increase is due to a growth spurt at the time of the sexual transition or due to the history of faster growth in sex changing individuals.[42] Larger males are able to stifle the growth of females and control environmental resources.

Social organization plays a large role in the changing of sex by the fish. It is often seen that a fish will change its sex when there is a lack of dominant male within the social hierarchy. The females that change sex are often those who attain and preserve an initial size advantage early in life. In either case, females which change sex to males are larger and often prove to be a good example of dimorphism.

In other cases with fish, males will go through noticeable changes in body size, and females will go through morphological changes that can only be seen inside of the body. For example, in sockeye salmon, males develop larger body size at maturity, including an increase in body depth, hump height, and snout length. Females experience minor changes in snout length, but the most noticeable difference is the huge increase in gonad size, which accounts for about 25% of body mass.[43]

Amphibians and reptiles

In amphibians and reptiles, the degree of sexual dimorphism varies widely among taxonomic groups. The sexual dimorphism in amphibians and reptiles may be reflected in any of the following: anatomy; relative length of tail; relative size of head; overall size as in many species of Vipers and Lizards; coloration as in many amphibians, snakes, and lizards, as well as in some chelonians; an ornament as in many newts and lizards; the presence of specific sex-related behaviour is common to many lizards; and vocal qualities which are frequently observed in frogs.

Anolis lizards show prominent size dimorphism with males typically being significantly larger than females. For instance, the average male Anolis sagrei was 53.4 mm vs. 40 mm in females.[44] Different sizes of the heads in anoles have been explained by differences in the estrogen pathway.[45]

Birds

Mandarin ducks, male (left) and female (right)

Sexual dimorphism in birds can be manifested in size or plumage differences between the sexes. Sexual size dimorphism varies among taxa with males typically being larger, though this is not always the case i.e. birds of prey and some species of flightless birds.[46] Plumage dimorphism, in the form of ornamentation or coloration, also varies, though males are typically the more ornamented or brightly colored sex.[47] Such differences have been attributed to the unequal reproductive contributions of the sexes.[48] This difference produces a stronger female choice since they have more risk in producing offspring. In some species, the male's contribution to reproduction ends at copulation, while in other species the male becomes the main caregiver. Plumage polymorphisms have evolved to reflect these differences and other measures of reproductive fitness, such as body condition[49] or survival.[50] The male phenotype sends signals to females who then choose the 'fittest' available male.

Sexual dimorphism is a product of both genetics and environmental factors. An example of sexual polymorphism determined by environmental conditions exists in the red-backed fairywren. Red-backed fairywren males can be classified into three categories during breeding season: black breeders, brown breeders, and brown auxiliaries.[49] These differences arise in response to the bird's body condition: if they are healthy they will produce more androgens thus becoming black breeders, while less healthy birds produce less androgens and become brown auxiliaries.[49] The reproductive success of the male is thus determined by his success during each year's non-breeding season, causing reproductive success to vary with each year's environmental conditions.

Migratory patterns and behaviors also influence sexual dimorphisms. This aspect also stems back to the size dimorphism in species. It has been shown that the larger males are better at coping with the difficulties of migration and thusly are more successful in reproducing when reaching the breeding destination.[51] When viewing this in an evolutionary standpoint many theories and explanations come to consideration. If these are the result for every migration and breeding season the expected results should be a shift towards a larger male population through sexual selection. Sexual selection is strong when the factor of environmental selection is also introduced. The environmental selection may support a smaller chick size if those chicks were born in an area that allowed them to grow to a larger size, even though under normal conditions they would not be able to reach this optimal size for migration. When the environment gives advantages and disadvantages of this sort. The strength of selection is weakened and the environmental forces are given greater morphological weight. The sexual dimorphism could also produce a change in timing of migration leading to differences in mating success within the bird population.[52] When the dimorphism produces that large of a variation between the sexes and between the members of the sexes multiple evolutionary effects can take place. This timing could eve lead to a speciation phenomenon if the variation becomes strongly drastic and favorable towards two different outcomes.

Sexual dimorphism is maintained by the counteracting pressures of natural selection and sexual selection. For example, sexual dimorphism in coloration increases the vulnerability of bird species to predation by European sparrowhawks in Denmark.[53] Presumably, increased sexual dimorphism means males are brighter and more conspicuous, leading to increased predation.[53] Moreover, the production of more exaggerated ornaments in males may come at the cost of suppressed immune function.[49] So long as the reproductive benefits of the trait due to sexual selection are greater than the costs imposed by natural selection, then the trait will propagate throughout the population. Reproductive benefits arise in the form of a larger number of offspring, while natural selection imposes costs in the form of reduced survival. This means that even if the trait causes males to die earlier, the trait is still beneficial so long as males with the trait produce more offspring than males lacking the trait. This balance keeps the dimorphism alive in these species and ensures that the next generation of successful males will also display these traits that are attractive to the females.

Such differences in form and reproductive roles often cause differences in behavior. As previously stated, males and females often have different roles in reproduction. The courtship and mating behavior of males and females are regulated largely by hormones throughout a bird's lifetime.[54] Activational hormones occur during puberty and adulthood and serve to 'activate' certain behaviors when appropriate, such as territoriality during breeding season.[54] Organizational hormones occur only during a critical period early in development, either just before or just after hatching in most birds, and determine patterns of behavior for the rest of the bird's life.[54] Such behavioral differences can cause disproportionate sensitivities to anthropogenic pressures.[55] Females of the whinchat in Switzerland breed in intensely managed grasslands.[55] Earlier harvesting of the grasses during the breeding season lead to more female deaths.[55] Populations of many birds are often male-skewed and when sexual differences in behavior increase this ratio, populations decline at a more rapid rate.[55] Also not all male dimorphic traits are due to hormones like testosterone, instead they are a naturally occurring part of development, for example plumage.[56]

Sexual dimorphism may also influence differences in parental investment during times of food scarcity. For example, in the Blue-footed Booby, the female chicks grow faster than the males, resulting in booby parents producing the smaller sex, the males, during times of food shortage. This then results in the maximization of parental lifetime reproductive success.[57]

Sexual dimorphism may also only appear during mating season, some species of birds only show dimorphic traits in seasonal variation. The males of these species will molt into a less bright or less exaggerated color during the off breading season.[58] This occurs because the species is more focused on survival than reproduction, causing a shift into a less ornate state.

Consequently, sexual dimorphism has important ramifications for conservation. However, sexual dimorphism is not only found in birds and is thus important to the conservation of many animals. Such differences in form and behavior can lead to sexual segregation, defined as sex differences in space and resource use.[59] Most sexual segregation research has been done on ungulates,[59] but such research extends to bats,[60] kangaroos,[61] and birds.[62] Sex-specific conservation plans have even been suggested for species with pronounced sexual segregation.[60]

Mammals

Just like in birds, the brains of many mammals, including humans, are significantly different for males and females of the species.[63] Both genes and hormones affect the formation of many animal brains before "birth" (or hatching), and also behaviour of adult individuals. Hormones significantly affect human brain formation, and also brain development at puberty. A 2004 review in Nature Reviews Neuroscience observed that "because it is easier to manipulate hormone levels than the expression of sex chromosome genes, the effects of hormones have been studied much more extensively, and are much better understood, than the direct actions in the brain of sex chromosome genes." It concluded that while "the differentiating effects of gonadal secretions seem to be dominant," the existing body of research "support the idea that sex differences in neural expression of X and Y genes significantly contribute to sex differences in brain functions and disease."[64]

Primates

Humans

Main articles: Sex differences in humans and Sex differences in human psychology

Top: Stylised illustration of humans on the Pioneer plaque, showing both male (left) and female (right).
Bottom: Comparison between male (left) and female (right) pelvises.

In humans, biological sex is determined by five factors present at birth: the presence or absence of a Y chromosome, the type of gonads, the sex hormones, the internal reproductive anatomy (such as the uterus in females), and the external genitalia.[65] Generally, the five factors are either all male or all female. Unexpected combinations cause intersex conditions.

The average differences between males and females include all the features related to reproduction. Sexual dimorphism among humans includes differentiation among gonads, internal genitals, external genitals, breasts, muscle mass, height, the endocrine (hormonal) systems and their physiological and behavioral effects. According to Clark Spencer Larsen, modern day Homo sapiens show a relatively narrow range of sexual dimorphism, with average body mass difference between the sexes being roughly equal to 15% (compared to most primates and anthropoids, ranging 50-55%). Ever since Charles Darwin's The Descent of Man and Selection in Relation to Sex in 1871 was published, there's been controversy regarding the social, cultural, and political significance of human sexual dimorphism. "Key points of discussion are how to interpret size dimorphism in humans and what inferences can be drawn about the evolution of human mating systems and social organization."[66]

The average basal metabolic rate is about 6 percent higher in adolescent males than females and increases to about 10 percent higher after puberty. Females tend to convert more food into fat, while males convert more into muscle and expendable circulating energy reserves. Aggregated data of absolute strength indicates that females have, on average, 40-60% the upper body strength of males, and 70-75% the lower body strength.[67] The difference in strength relative to body mass is less pronounced in trained individuals. In Olympic weightlifting, male records vary from 5.5× body mass in the lowest weight category to 4.2× in the highest weight category, while female records vary from 4.4× to 3.8×, a weight adjusted difference of only 10-20%, and an absolute difference of about 30% (i.e. 472 kg vs 333 kg for unlimited weight classes)(see Olympic weightlifting records). A study, carried about by analyzing annual world rankings from 1980–1996, found that males' running times were, on average, 11% faster than females'.[68]

Males, on average, are taller than females. In the United States, adult males are, on average, 4% taller[69] and 8% heavier[70] than adult females.

Males typically have larger tracheae and branching bronchi, with about 30 percent greater lung volume per body mass. On average, males have larger hearts, 10 percent higher red blood cell count, higher hemoglobin, hence greater oxygen-carrying capacity. They also have higher circulating clotting factors (vitamin K, prothrombin and platelets). These differences lead to faster healing of wounds and higher peripheral pain tolerance. Males also have more white blood cells (stored and circulating), more granulocytes and B and T lymphocytes. Additionally, they produce more antibodies at a faster rate than females. Hence they develop fewer infectious diseases and succumb for shorter periods[71]

Females typically .[71] Ethologists argue that females, interacting with other females and multiple offspring in social groups, have experienced such traits as a selective advantage.[72][73][74][75][76]

Considerable discussion in academic literature concerns potential evolutionary advantages associated with sexual competition (both intrasexual and intersexual) and short- and long-term sexual strategies.[77]

According to Daly and Wilson, "The sexes differ more in human beings than in monogamous mammals, but much less than in extremely polygamous mammals."[78] One proposed explanation is that human sexuality has developed more in common with its close relative the bonobo, who have similar sexual dimorphism and which are polygynandrous and use recreational sex to reinforce social bonds and reduce aggression.[79]

In the human brain, a difference between sexes was observed in the transcription of the PCDH11X/Y gene pair unique to Homo sapiens.[80] Sexual differentiation in the human brain from the default female state is triggered by testosterone from the fetal testis. Testosterone is converted to estrogen in the brain through the action of the enzyme aromatase. Testosterone acts on many brain areas, including the SDN-POA, to create the masculinized brain pattern. [81] Female brains may be shielded from the masculinizing effects of estrogen through the action of sex-hormone binding globulin and a-fetoprotein. [82] The relationship between sex differences in the brain and human behavior is a subject of controversy in psychology and society at large.[83][84] Many females tend to have a higher ratio of gray matter in the left hemisphere of the brain in comparison to males.[85][86] However, on average, males have larger brains than females, and when adjusted for total brain volume the gray matter differences between sexes is almost nonexistent. Thus, the percentage of gray matter appears to be more related to brain size than it is to sex.[87][88] Differences in brain physiology between sexes do not necessarily relate to differences in intellect. Haier et al. found in a 2004 study that "men and women apparently achieve similar IQ results with different brain regions, suggesting that there is no singular underlying neuroanatomical structure to general intelligence and that different types of brain designs may manifest equivalent intellectual performance".[89] (See the sex and intelligence article for more on this subject.)

The bed nucleus of the stria terminalis shows strong sexual dimorphism, being twice as large in males as in females.

Cells

Phenotypic differences between sexes are evident even in cultured cells from tissues.[90] For example, female muscle-derived stem cells have a better muscle regeneration efficiency than male ones.[91] There are reports of several metabolic differences between male and female cells[92] and they also respond to stress differently.[93]

See also

References

Notes

  1. ↑ 1.0 1.1 A. Johnsen, K. Delhey, S. Andersson & B. Kempenaers (2003). "Plumage colour in nestling blue tits: sexual dichromatism, condition dependence and genetic effects" (PDF). Proceedings of the Royal Society B 270 (1521): 1263–1270. doi:10.1098/rspb.2003.2375. JSTOR 3558810. PMC 1691364. PMID 12816639.
  2. ↑ Bill Branch (1988). Bill Branch's Field Guide to the Snakes and Other Reptiles of Southern Africa. Cape Town: Struik. ISBN 978-0-86977-639-1.
  3. ↑ 3.0 3.1 Andersson 1994
  4. ↑ Amotz Zahavi (1975). "Mate selection – a selection for a handicap" (PDF). Journal of Theoretical Biology 53 (1): 205–214. doi:10.1016/0022-5193(75)90111-3. PMID 1195756.
  5. ↑ T. Slagsvold & J. T. Lifjeld (1985). "Variation in plumage colour of the Great tit Parus major in relation to habitat, season and food". Journal of Zoology 206 (3): 321–328. doi:10.1111/j.1469-7998.1985.tb05661.x.
  6. ↑ Stefan Andersson, Jonas Örnborg & Malte Andersson (1998). "Ultraviolet sexual dimorphism and assortative mating in blue tits". Proceedings of the Royal Society B: Biological Sciences 265 (1395): 445–450. doi:10.1098/rspb.1998.0315. PMC 1688915.
  7. ↑ Sarah Hunt, Andrew T. D. Bennett, Innes C. Cuthill & Richard Griffiths (1998). "Blue tits are ultraviolet tits". Proceedings of the Royal Society B: Biological Sciences 265 (1395): 451–455. doi:10.1098/rspb.1998.0316. JSTOR 50814. PMC 1688906.
  8. ↑ J. C. Senar, J. Figuerola & J. Pascual (2002). "Brighter yellow blue tits make better parents". Proceedings of the Royal Society B: Biological Sciences 269 (1488): 257–261. doi:10.1098/rspb.2001.1882. PMC 1690890. PMID 11839194.
  9. ↑ George A. Lozano (1994). "Carotenoids, parasites, and sexual selection" (PDF). Oikos 70 (2): 309–311. doi:10.2307/3545643. JSTOR 3545643.
  10. ↑ Michael J. Ryan & A. Stanley Rand (1993). "Species recognition and sexual selection as a unitary problem in animal communication" (PDF). Evolution 47 (2): 647–657. doi:10.2307/2410076.
  11. ↑ 11.0 11.1 S. A. Collins & S. T. Luddem (2002). "Degree of male ornamentation affects female preference for conspecific versus heterospecific males" (PDF). Proceedings of the Royal Society B 269 (1487): 111–117. doi:10.1098/rspb.2001.1864. JSTOR 3067942. PMC 1690881. PMID 11798425.
  12. ↑ Giacomello, Eva (2006). "A male sexually dimorphic trait provides antimicrobials to eggs in blenny fish". Biology Letters 2: 330–333. doi:10.1098/rsbl.2006.0492.
  13. ↑ Deborah Charlesworth & Judith E. Mank (2010). "The birds and the bees and the flowers and the rrees: lessons from genetic mapping of sex determination in plants and animals". Genetics 186 (1): 9–31. doi:10.1534/genetics.110.117697.
  14. ↑ G. A. Parker (1982). "Why are there so many tiny sperm? Sperm competition and the maintenance of two sexes". Journal of Theoretical Biology 96 (2): 281–294. doi:10.1016/0022-5193(82)90225-9.
  15. ↑ Jiang-Nan Yang (2010). "Cooperation and the evolution of anisogamy". Journal of Theoretical Biology 264 (1): 24–36. doi:10.1016/j.jtbi.2010.01.019. PMID 20097207.
  16. ↑ G. Bell (1985). "On the function of flowers". Proceedings of the Royal Society B: Biological Sciences 224 (1235): 223–266. Bibcode:1985RSPSB.224..223B. doi:10.1098/rspb.1985.0031. JSTOR 36033.
  17. ↑ Futuyma 2005, p. 330
  18. ↑ Futuyma 2005, p. 331
  19. ↑ Futuyma 2005, p. 332
  20. ↑ 20.0 20.1 Ridley 2004, p. 328
  21. ↑ Futuyma 2005, p. 335
  22. ↑ Ridley 2004, p. 330
  23. ↑ Ridley 2004, p. 332
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