Sexual dimorphism

From Wikipedia, the free encyclopedia - View original article

 
Jump to: navigation, search
Female (left) and Male (Right) Common Pheasant, illustrating the dramatic difference in both color and size between sexes

Sexual dimorphism is a phenotypic difference between males and females of the same species, meaning that there are obvious differences between the male and female of the species. The main differences are the presence or absence of reproductive organs. However, more obvious differences are often secondary sex characteristics, such as size differences in males and females, ornamentation and behavior.

Examples[edit]

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 / coloration[edit]

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.[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[edit]

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[edit]

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[edit]

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 dimorphism 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 female 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 larger females than males[edit]

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. Vollrath and 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. In this species, females are substantially larger than males. They differ in body weight, skull measurement, and forearm length.[25] The difference in size is believed to be caused by natural selection for a large female size due to a fecundity advantage. The interaction between the sexes and energetic needs such as time and energy required 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 that of the male who only bears the cost of making sperm. The fecundity advantage hypothesis states, that a big mother is able to produce more offspring and give those offspring more favorable conditions to ensure their survival. This is true for most ectotherms. Another reason why females are believed to be larger is due to the fact that they provide parental care for a substantial amount of time while the offspring matures. The time of gestation and lactation is fairly long in the M. nigricans, where females suckle their offspring until 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. In addition to the hypothesis that explains an advantage of large female size, it is hypothesized that smaller male size is an adaptation for males to increase maneuverability and agility. This selection for agility in flying is a helpful adaptation which allows males to better compete 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]

Plants[edit]

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[edit]

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[edit]

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[edit]

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] 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 house finch. House finch 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.

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.[51] Presumably, increased sexual dimorphism means males are brighter and more conspicuous, leading to increased predation.[51] 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.

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.[52] Activational hormones occur during puberty and adulthood and serve to 'activate' certain behaviors when appropriate, such as territoriality during breeding season.[52] 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.[52] Such behavioral differences can cause disproportionate sensitivities to anthropogenic pressures.[53] Females of the whinchat in Switzerland breed in intensely managed grasslands.[53] Earlier harvesting of the grasses during the breeding season lead to more female deaths.[53] Populations of many birds are often male-skewed and when sexual differences in behavior increase this ratio, populations decline at a more rapid rate.[53]

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 them results in the maximization of parental lifetime reproductive success.[54]

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.[55] Most sexual segregation research has been done on ungulates,[55] but such research extends to bats,[56] kangaroos,[57] and birds.[58] Sex-specific conservation plans have even been suggested for species with pronounced sexual segregation.[56]

Mammals[edit]

Just like in birds, the brains of many mammals, including humans, are significantly different for males and females of the species.[59] 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."[60]

Primates[edit]

Humans[edit]

Pioneer plaque
Male pelvis
Female pelvis

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

Obvious differences between males and females include all the features related to reproductive role, notably the endocrine (hormonal) systems and their physiological and behavioral effects. Such undisputed sexual dimorphism includes differentiation among gonads, internal genitals, external genitals, breasts, muscle mass, and height.

The 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 40-60% the upper body strength of males, and 70-75% the lower body strength.[61] 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× (see Olympic weightlifting records). A study, carried about by analysing annual world rankings from 1980–1996, found that males' running times were roughly 11% faster than females'.[62]

Females are taller (on average) than males in early adolescence, but males (on average) surpass them in height in later adolescence and adulthood. In the United States, adult males are, on average, 4% taller[63] and 8% heavier[64] than adult females.

Males typically have larger tracheae and branching bronchi, with about 30 percent greater lung volume per body mass. They 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.[65]

Females typically 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 males. Hence they develop fewer infectious diseases and succumb for shorter periods.[65] Ethologists argue that females, interacting with other females and multiple offspring in social groups, have experienced such traits as a selective advantage.[66][67][68][69][70]

Considerable discussion in academic literature concerns potential evolutionary advantages associated with sexual competition (both intrasexual and intersexual) and short- and long-term sexual strategies.[71]

According to Daly and Wilson, "The sexes differ more in human beings than in monogamous mammals, but much less than in extremely polygamous mammals."[72][unreliable source?] 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.[73]

In the human brain, a difference between sexes was observed in the transcription of the PCDH11X/Y gene pair unique to Homo sapiens.[74] The relationship between sex differences in the brain and human behavior is a subject of controversy in psychology and society at large.[75][76] Females on average have a higher percentage of gray matter in comparison to males.[77][78] However, males have larger brains on average than females, and when adjusted for total brain volume the gray matter differences between sexes is small or nonexistent. Thus, the percentage of gray matter appears to be more related to brain size than it is to sex.[79][80] 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".[81] (See the sex and intelligence article for more on this subject.)

Cells[edit]

Phenotypic differences between sexes are evident even in cultured cells from tissues.[82] For example, female muscle-derived stem cells have a better muscle regeneration efficiency than male ones.[83] There are reports of several metabolic differences between male and female cells[84] and they also respond to stress differently.[85]

See also[edit]

References[edit]

Notes[edit]

  1. ^ a b 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. ^ a b 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. 
  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. ^ a b 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. 
  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. ^ a b Ridley 2004, p. 328
  21. ^ Futuyma 2005, p. 335
  22. ^ Ridley 2004, p. 330
  23. ^ Ridley 2004, p. 332
  24. ^ a b Fritz Vollrath & Geoff A. Parker (1992). "Sexual dimorphism and distorted sex ratios in spiders". Nature 360 (6400): 156–159. Bibcode:1992Natur.360..156V. doi:10.1038/360156a0. 
  25. ^ R. I. Bornholdt, L. R. Oliveira & M. E. Fabián (2008). "Sexual size dimorphism in Myotis nigricans (Schinz, 1821) (Chiroptera: Vespertilionidae) from south Brazil" (PDF). Brazilian Journal of Biology 68 (4): 897–904. doi:10.1590/S1519-69842008000400028. PMID 19197511. 
  26. ^ Virginia Hayssen & T. H. Kunz (1996). "Allometry of litter mass in bats: comparisons with maternal size, wing morphology, and phylogeny" (PDF). Journal of Mammalogy 77 (2): 476–490. doi:10.2307/1382823. JSTOR 1382823. 
  27. ^ Göran Arnqvist, Therésa M. Jones & Mark A. Elgar (2003). "Insect behaviour: reversal of sex roles in nuptial feeding" (PDF). Nature 424 (6947): 387. Bibcode:2003Natur.424..387A. doi:10.1038/424387a. PMID 12879056. [dead link]
  28. ^ A. Jonathan Shaw (2000). "Population ecology, population genetics, and microevolution". In A. Jonathan Shaw & Bernard Goffinet. Bryophyte Biology. Cambridge: Cambridge University Press. pp. 379–380. ISBN 978-0-521-66097-6. 
  29. ^ a b Schuster, Rudolf M. (1984). "Comparative Anatomy and Morphology of the Hepaticae". New Manual of Bryology 2. Nichinan, Miyazaki, Japan: The Hattori botanical Laboratory. p. 891. 
  30. ^ Howard A. Crum & Lewis E. Anderson (1980). Mosses of Eastern North America 1. New York: Columbia University Press. p. 196. ISBN 978-0-231-04516-2. 
  31. ^ D. Briggs (1965). "Experimental taxonomy of some British species of genus Dicranum". New Phytologist 64 (3): 366–386. doi:10.1111/j.1469-8137.1965.tb07546.x. JSTOR 2430169. 
  32. ^ Renner, Susanne; Ricklefs, Robert E (1995). "Dioecy and its correlates in the flowering plants". Americal Journal of Botany 82 (5): 596–606. doi:10.2307/2445418. 
  33. ^ Romero, Gustavo; Nelson, Craig E. (1986). "Sexual Dimorphism in Catasetum Orchids: Forcible Pollen Emplacement and Male Flower Competition". Science 232 (4757): 1538–1540. Bibcode:1986Sci...232.1538R. doi:10.1126/science.232.4757.1538. 
  34. ^ "Eel Grass (aka wild celery, tape grass)". University of Massachusetts. 
  35. ^ Friedman, Jannice; Barrett, Spencer (2009). "Wind of change: new insights on the ecology and evolution of pollination and mating in wind-pollinated plants". Annals of Botany 103: 1515–1527. doi:10.1093/aob/mcp035. 
  36. ^ Geber, Monica A. (1999). Gender and sexual dimorphism in flowering plants. Berlin: Springer. ISBN 3-540-64597-7.  p. 206
  37. ^ Kazutaka Ota, Masanori Kohda & Tetsu Sato (2010). "Unusual allometry for sexual size dimorphism in a cichlid where males are extremely larger than females". Journal of Biosciences 35 (2): 257–265. doi:10.1007/s12038-010-0030-6. 
  38. ^ Tetsu Sato (1994). "Active accumulation of spawning substrate: a determinant of extreme polygyny in a shell-brooding cichlid fish". Animal Behaviour 48 (3): 669–678. doi:10.1006/anbe.1994.1286. 
  39. ^ Dolores Schütz & Michael Taborsky (2005). "Mate choice and sexual conflict in the size dimorphic water spider Argyroneta aquatica (Araneae: Argyronetidae)" (PDF). Journal of Arachnology 33 (3): 767–775. doi:10.1636/S03-56.1. 
  40. ^ Mark I. McCormick, Christopher A. Ryen, Philip L. Munday, Stefan P. W. Walker (2010). "Differing mechanisms underlie sexual size-dimorphism in two populations of a sex-changing fish". In Briffa, Mark. PLoS One 5 (5): e10616. Bibcode:2010PLoSO...510616M. doi:10.1371/journal.pone.0010616. PMC 2868897. PMID 20485547. 
  41. ^ Robert R. Warner (1998). "Sex change and the size-advantage model". Trends in Ecology and Evolution 3 (6): 133–136. doi:10.1016/0169-5347(88)90176-0. PMID 21227182. 
  42. ^ S. Adams & A. J. Williams (2001). "A preliminary test of the transitional growth spurt hypothesis using the protogynous coral trout Plectropomus maculatus". Journal of Fish Biology 59 (1): 183–185. doi:10.1111/j.1095-8649.2001.tb02350.x. 
  43. ^ Hendry, Andrew P.; Ole K. Berg (1999). "Secondary sexual characters, energy use, senescence, and the cost of reproduction in sockeye salmon". Canadian Journal of Zoology 77: 1663–1675. doi:10.1139/cjz-77-11-1663. 
  44. ^ Butler, M. A.;, et al. (2000) THE RELATIONSHIP BETWEEN SEXUAL SIZE DIMORPHISM AND HABITAT USE IN GREATER ANTILLEAN ANOLIS LIZARDS. Evolution, 54(1): 259–272
  45. ^ Sanger TJ, Seav SM, Tokita M, Langerhans RB, Ross LM, Losos JB, Abzhanov A. 2014. The oestrogen pathway underlies the evolution of exaggerated male cranial shapes inAnolis lizards. Proceedings of the Royal Society B 281:20140329. doi:10.1098/rspb.2014.0329
  46. ^ Andersson 1994, p. 269
  47. ^ K. J. McGraw, G. E. Hill, R. Stradi & R. S. Parker (2002). "The effect of dietary carotenoid access on sexual dichromatism and plumage pigment composition in the American goldfinch" (PDF). Comparative Biochemistry and Physiology Part B-Biochemistry and Molecular Biology 131 (2): 261–269. doi:10.1016/S1096-4959(01)00500-0. [dead link]
  48. ^ I. P. F. Owens & I. R. Hartley (1998). "Sexual dimorphism in birds: why are there so many different forms of dimorphism?". Proceedings of the Royal Society B 265 (1394): 397–407. doi:10.1098/rspb.1998.0308. JSTOR 50849. PMC 1688905. 
  49. ^ a b c d Willow R. Lindsay, Michael S. Webster, Claire W. Varian & Hubert Schwabl (2009). "Plumage colour acquisition and behaviour are associated with androgens in a phenotypically plastic bird". Animal Behaviour 77 (6): 1525–1532. doi:10.1016/j.anbehav.2009.02.027. 
  50. ^ Marion Petrie (1994). "Improved growth and survival of offspring of peacocks with more elaborate trains" (PDF). Nature 371 (6498): 598–599. Bibcode:1994Natur.371..598P. doi:10.1038/371598a0. 
  51. ^ a b Anders Pape Møller & Jan Tøttrup Nielsen (2006). "Prey vulnerability in relation to sexual coloration of prey" (PDF). Behavioral Ecology and Sociobiology 60 (2): 227–233. doi:10.1007/s00265-006-0160-x. 
  52. ^ a b c Elizabeth Adkins-Regan (2007). "Hormones and the development of sex differences in behavior". Journal of Ornithology 148 (Supplement 1): S17–S26. doi:10.1007/s10336-007-0188-3. 
  53. ^ a b c d Martin U. Grüebler, Heidi Schuler, Mathis Müller, Reto Spaar, Petra Horch & Beat Naef-Daenzer (2008). "Female biased mortality caused by anthropogenic nest loss contributes to population decline and adult sex ratio of a meadow bird". Biological Conservation 141 (12): 3040–3049. doi:10.1016/j.biocon.2008.09.008. 
  54. ^ Velando, Alberto (2002). "Experimental Manipulation of Maternal Effort Produces Differential Effects in Sons and Daughters: Implications for Adaptive Sex Ratios in the Blue-footed Booby". Behavioral Ecology 14 (4). 
  55. ^ a b Martin B. Main (2008). "Reconciling competing ecological explanations for sexual segregation in ungulates". Ecology 89 (3): 693–704. doi:10.1890/07-0645.1. PMID 18459333. 
  56. ^ a b Kamran Safi, Barbara König & Gerald Kerth (2007). "Sex differences in population genetics, home range size and habitat use of the parti-colored bat (Vespertilio murinus, Linnaeus 1758) in Switzerland and their consequences for conservation". Biological Conservation 137 (1): 28–36. doi:10.1016/j.biocon.2007.01.011. 
  57. ^ G. Coulson, A. M. MacFarlane, S. E. Parsons & J. Cutter (2006). "Evolution of sexual segregation in mammalian herbivores: kangaroos as marsupial models" (PDF). Australian Journal of Zoology 54 (3): 217–224. doi:10.1071/ZO05062. 
  58. ^ Jacob González-Solís, John P. Croxall & Andy G. Wood (2000). "Sexual dimorphism and sexual segregation in foraging strategies of northern giant petrels, Macronectes halli, during incubation". Oikos 90 (2): 390–398. doi:10.1034/j.1600-0706.2000.900220.x. 
  59. ^ Robert W. Goy and Bruce S. McEwen (1980). Sexual Differentiation of the Brain: Based on a Work Session of the Neurosciences Research Program. Boston: MIT Press. ISBN 978-0-262-57207-1. 
  60. ^ Arthur P. Arnold (2004). "Sex chromosomes and brain gender". Nature Reviews Neuroscience 5 (9): 701–708. doi:10.1038/nrn1494. PMID 15322528. 
  61. ^ "Strength training for female athletes: A position paper: Part 1". NSCA 11 (4). 1989. [dead link]
  62. ^ Phillip B. Sparling, Elizabeth M. O'Donnell & Teresa K. Snow (1998). "The gender difference in distance running performance has plateaued: an analysis of world rankings from 1980 to 1996". Medicine & Science in Sports & Exercise 30 (12): 1725–1729. doi:10.1097/00005768-199812000-00011. PMID 9861606. 
  63. ^ "National Health Statistics Reports". National Health Statistics Reports 10. October 22, 2008. Retrieved 21 April 2012. 
  64. ^ "United States National Health and Nutrition Examination Survey, 1999–2002" (PDF). Retrieved 2014-05-01. 
  65. ^ a b Alfred Glucksman (1981). Sexual Dimorphism in Human and Mammalian Biology and Pathology. Academic Press. pp. 66–75. ISBN 978-0-12-286960-0. OCLC 7831448. 
  66. ^ Jo Durden-Smith & Diane deSimone (1983). Sex and the Brain. New York: Arbor House. ISBN 978-0-87795-484-2. 
  67. ^ Gersh, Eileen S.; Gersh, Isidore (1981). Biology of Women. Baltimore: University Park Press (original from the University of Michigan). ISBN 0839116225. 
  68. ^ Jay H. Stein (1987). Internal Medicine (2nd ed.). Boston: Little, Brown. ISBN 978-0-316-81236-8. 
  69. ^ M. McLaughlin & T. Shryer (8 August 1988). "Men vs women: the new debate over sex differences". U.S. News & World Report: 50–58. 
  70. ^ B. S. McEwen (1981). "Neural gonadal steroid actions". Science 210 (4488): 1303–1311. Bibcode:1981Sci...211.1303M. doi:10.1126/science.6259728. PMID 6259728. 
  71. ^ David M. Buss (2007). "The evolution of human mating" (PDF). Acta Psychologica Sinica 39 (3): 502–512. 
  72. ^ Martin Daly & Margo Wilson (1996). "Evolutionary psychology and marital conflict". In David M. Buss & Neil M. Malamuth. Sex, Power, Conflict: Evolutionary and Feminist Perspectives. Oxford University Press. p. 13. ISBN 978-0-19-510357-1. 
  73. ^ Christopher Ryan & Cacilda Jethá (2010). Sex at Dawn: The Prehistoric Origins of Modern Sexuality. Harper. ISBN 978-0-06-170780-3. 
  74. ^ Alexandra M. Lopes, Norman Ross, James Close, Adam Dagnall, António Amorim & Timothy J. Crow (2006). "Inactivation status of PCDH11X: sexual dimorphisms in gene expression levels in brain". Human Genetics 119 (3): 1–9. doi:10.1007/s00439-006-0134-0. PMID 16425037. 
  75. ^ Cordelia Fine (August 2010). Delusions of Gender: How Our Minds, Society, and Neurosexism Create Difference (1st ed.). W. W. Norton & Company. ISBN 978-0-393-06838-2. 
  76. ^ Rebecca Jordan-Young (September 2010). Brain Storm: The Flaws in the Science of Sex Differences. Harvard University Press. ISBN 978-0-674-05730-2. 
  77. ^ Lisbeth Marner, Jens R. Nyengaard, Yong Tang & Bente Pakkenberg (2003). "Marked loss of myelinated nerve fibers in the human brain with age". The Journal of Comparative Neurology 462 (2): 144–152. doi:10.1002/cne.10714. PMID 12794739. 
  78. ^ Ruben C. Gur, Bruce I. Turetsky, Mie Matsui, Michelle Yan, Warren Bilker, Paul Hughett & Raquel E. Gur (1999). "Sex differences in brain gray and white matter in healthy young adults: correlations with cognitive performance". The Journal of Neuroscience 19 (10): 4065–4072. PMID 10234034. 
  79. ^ Christiana M. Leonard, Stephen Towler, Suzanne Welcome, Laura K. Halderman, Ron Otto, Mark A. Eckert & Christine Chiarello (2008). "Size matters: cerebral volume influences sex differences in neuroanatomy". Cerebral Cortex 18 (12): 2920–2931. doi:10.1093/cercor/bhn052. PMC 2583156. PMID 18440950. 
  80. ^ Eileen Lüders, Helmuth Steinmetz & Lutz Jäncke (2002). "Brain size and grey matter volume in the healthy human brain". NeuroReport 13 (17): 2371–2374. doi:10.1097/00001756-200212030-00040. PMID 12488829. 
  81. ^ Richard J. Haier, Rex E. Jung, Ronald A. Yeo, Kevin Head & Michael T. Alkire (2005). "The neuroanatomy of general intelligence: sex matters" (PDF). NeuroImage 25 (1): 320–327. doi:10.1016/j.neuroimage.2004.11.019. PMID 15734366. [dead link]
  82. ^ Pollitzer, E. (2013). "Biology: Cell sex matters". Nature 500 (7460): 23–24. doi:10.1038/500023a. PMID 23903733.  edit
  83. ^ Deasy, B. M.; Lu, A.; Tebbets, J. C.; Feduska, J. M.; Schugar, R. C.; Pollett, J. B.; Sun, B.; Urish, K. L.; Gharaibeh, B. M.; Cao, B.; Rubin, R. T.; Huard, J. (2007). "A role for cell sex in stem cell-mediated skeletal muscle regeneration: Female cells have higher muscle regeneration efficiency". The Journal of Cell Biology 177 (1): 73–86. doi:10.1083/jcb.200612094. PMC 2064113. PMID 17420291.  edit
  84. ^ Mittelstrass, K.; Ried, J. S.; Yu, Z.; Krumsiek, J.; Gieger, C.; Prehn, C.; Roemisch-Margl, W.; Polonikov, A.; Peters, A.; Theis, F. J.; Meitinger, T.; Kronenberg, F.; Weidinger, S.; Wichmann, H. E.; Suhre, K.; Wang-Sattler, R.; Adamski, J.; Illig, T. (2011). "Discovery of Sexual Dimorphisms in Metabolic and Genetic Biomarkers". In McCarthy, Mark I. PLoS Genetics 7 (8): e1002215. doi:10.1371/journal.pgen.1002215. PMC 3154959. PMID 21852955.  edit
  85. ^ Penaloza, C.; Estevez, B.; Orlanski, S.; Sikorska, M.; Walker, R.; Smith, C.; Smith, B.; Lockshin, R. A.; Zakeri, Z. (2009). "Sex of the cell dictates its response: Differential gene expression and sensitivity to cell death inducing stress in male and female cells". The FASEB Journal 23 (6): 1869. doi:10.1096/fj.08-119388.  edit

Bibliography[edit]

Further reading[edit]

External links[edit]