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Precopulatory Reproductive Strategies
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Tommaso Pizzari University of Stockholm, Björnlunda, Sweden
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Advanced
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doi:10.1038/npg.els.0003663
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The quality and
number of young produced by an organism contribute to the spread of its
genes, and thus its evolutionary performance depends crucially on its
reproductive success. Precopulatory reproductive
strategies are the first step towards such success.
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Introduction
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Reproduction is the ultimate evolutionary
goal of an organism because it allows the transmission of its genes to
future generations. Both the quality and the number of young produced by an
individual in a lifetime contribute to the spread of its genes, and thus
the evolutionary success of an individual depends crucially on its
reproductive success. Alleles (variants created by mutation of particular
genes) coding for behavioural and morphological
traits that convey a reproductive advantage increase in frequency because
they are favoured by sexual selection, allowing more
efficient reproductive strategies to evolve. Both males and females
influence reproductive success at different stages of a reproductive event:
(1) before insemination, (2) after insemination and before fertilization,
and (3) after fertilization. Precopulatory
reproductive strategies are mechanisms occurring before insemination
through which males and females influence the success of the current
reproductive event by biasing the probability with which individual females
obtain sperm from individual males. Male and female precopulatory
strategies often interact in a complex way to determine the outcome of
inseminations, making it difficult to partition the effect of individual
strategies on variation in copulation success, and to establish the extent
to which each sex controls this stage of reproduction. See also: Reproductive strategies
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Male Polygyny
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Male reproductive success increases mainly
with the number of eggs fertilized, and because males produce more sperm
than females produce eggs, the number of eggs fertilized by a male
generally depends on how many females he inseminates. Therefore, the main
goal of male precopulatory strategies is to
distribute sperm between multiple females in a way that will maximize the
number of eggs fertilized. Male copulation success is usually determined by
two mechanisms: competition among males for access to females, and male
manipulation of the female decision to copulate through seduction or sexual
coercion.
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Males also compete fiercely to obtain
privileged access to females and copulation opportunities. Often it is the
variation in competitive ability and social status which determines
asymmetries in access to copulation opportunities among males, dominant
males having typically a higher probability of copulating with any given
female than their subordinates. In a number of species males defend a
territory where they attract females with courtship displays, and access to
females is mediated by the competition for the best territories. This is
particularly relevant in species where females depend on the quality of
resources contained in a male’s territory to reproduce successfully.
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Males produce courtship displays, which
range from the release of pheromones to complex behavioural
patterns and the exhibition of elaborate sexual ornaments, to manipulate
female propensity to copulate (Table 1). Typically, females
sample different males and rank their displays according to some aesthetic
or sensory criteria. Female propensity to copulate with a male is
influenced by the quality of his display. The more intense, elaborate or
complex displays often appear to produce more successful stimuli and result
in more copulation opportunities for the male. However, the relationship
between the intensity of male display and female propensity to copulate has
seldom been studied in detail and should not be assumed to be always
directional. See also: Sexual selection
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Male displays can be complex and generate
a whole suite of stimuli. In the fruitfly, Drosophila
melanogaster, male display comprises several
steps: males tap the female abdomen with their forelegs, vibrate their
wings to generate courtship songs, lick the female genitalia, and finally
attempt to mount the female (Hall, 1994). The extreme
complexity of male sexual ornaments and displays is symptomatic of intense
competition among males to monopolize female attention and manipulate
female propensity to copulate. A widespread mechanism through which males
manipulate female copulation decisions is the exploitation of female
sensory predisposition towards some stimuli. Perception is often biased
towards specific stimuli and females may be attracted by male displays
producing such stimuli. For example, in the blind water mite, Neumania papillator,
females feed on small copepods, which they detect from the vibrations
generated in the water by the crustaceans. The courtship displays of male
water mites exploit this female bias for water vibrations. Males wave their
legs in front of females, generating vibrations similar to those generated
by copepods. This triggers the attention of the female. The male then
deposits his spermatophores and again waves its
legs in front of the female (Proctor, 1991). The primary
function of male courtship displays is to signal females the location of
sexual partners of the same species. Whether male displays also provide
females with reliable cues of male phenotypic and/or genetic quality, thus
allowing females to select copulation partners delivering relatively high
benefits, is still unresolved (see below).
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In a number of species female reproductive
success is influenced by resources, like food or a territory in which to
raise the young, which are provided by males. In these cases females are
expected to evaluate males on the basis of the quality of the resources
offered, and males are under selective pressure to deliver better resources
than their competitors. However, male cheating may evolve and male displays
may not necessarily be honest signals of the resource quality (in the same
way in which commercial advertisements do not necessarily honestly portray
the quality of a product). For example, before or during copulation, males
of several species (especially insects and some birds) feed females either
with the gift of prey or with nutrients contained in their ejaculates. This
courtship feeding often improves female fecundity, egg weight and offspring
survival, and females preferentially copulate with males that provide the
largest nutritional benefits. However, in some species male gifts have
become purely symbolic and devoid of real nutritive value. In such cases
females may still be attracted by such gifts if they maintain a sensory
predisposition towards male gifts evolved when these gifts were associated
with real nutritional value. See also: Signalling and reception
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Alternative male reproductive
strategies
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Seducing females with courtship displays
is not the only precopulatory strategy adopted by
males. Less attractive males may resort to alternative strategies to increase
the number of females that they inseminate. Less attractive males are
therefore under selective pressure to circumvent female resistance and
coerce females into copulating. Sexual coercion is a widespread male
strategy that is particularly important to those male phenotypes that are
usually avoided or resisted by females. In many species males have evolved
traits that facilitate forced copulation; in others males may display
aggression towards females that resist their sexual advances to discourage
further resistance and increase the probability of successfully
inseminating them in the future, a strategy referred to as sexual
punishment. Less attractive males may resort to alternative strategies to
increase the number of females that they inseminate. In some species two
types of male strategies co-occur in populations: males can either defend a territory, attract females through
sexual display and guard them from other males (territorial males); or
sneak into the territory of other males to copulate with their females
(sneaker, floater or satellite males).
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What maintains polymorphism of male precopulatory strategies in natural population is
unclear. However, it is increasingly obvious that alternative strategies
are associated with different costs and benefits. Territoriality imposes
major investments: the competition for a territory, its defence, and the
protection of females from the advances of other males. In turn,
territoriality translates into privileged access to females. Sneaker
strategies rely on cryptic behaviours, the
ability to move quickly through the territories of other males, to copulate
with females, avoiding the interference of territorial males and overcoming
female resistance against them. Sneaker males do not need to invest heavily
in the ability to compete over territories and females, but their sperm
will invariably compete with the sperm of territorial males for the
fertilization of eggs. In the bluegill sunfish, Lepomis
macrochirus, three male strategies occur: (1)
territorial males, which build nests, court females and provide solitary
parental care for the embryos, (2) ‘sneakers’, which dart in and out of
nests of territorial males to ejaculate between spawning pairs of
territorial males and their females; and (3) ‘satellites’, which mimic
females in order to approach the nests of territorial males and ejaculate
between spawning pairs. Territorial males are larger than,
and socially dominant over, both sneakers and satellites but these are more
efficient at fertilizing eggs (Fu et al., 2001). In
some species, males plastically adopt one or the other precopulatory
strategy according to both current condition (e.g. energy reserves, social
status and age) and social factors (e.g. frequency of different strategies
currently occurring in the population, as the success of sneakers depends
upon the availability of territorial males, and availability of females).
In other species, male strategies are genetically determined and different
male genotypes consistently adopt different strategies. In this case
different male strategies may coexist at evolutionarily stable frequency
equilibrium where such strategies have similar fitness payoffs.
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Male cooperation
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Competition between males over copulation
opportunities is typically a powerful selective force; however, under
particular circumstances it may pay some males to cooperate rather than
compete to obtain more copulations. This is
generally true when the benefits derived by cooperation (e.g. increased
copulation opportunities) outweigh the costs of sharing females with other
males. For example, by cooperating with each other, males may attract more
females by producing more powerful displays or may coerce females into
copulating more efficiently. One condition that facilitates the evolution
of cooperation between males is genetic relatedness. By helping related
males to copulate, a male contributes indirectly to his genetic
representation in the next generation. In lekking
species, where males do not care for the offspring and display concentrated
in arenas to attract females, a larger concentration of displaying males
generally attracts more females, and males need to join each other to
reinforce their advertisement. There is increasing evidence that in lekking species related males tend to associate with
each other and to cooperate to attract females.
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Female Choice of
Partners
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The production of eggs is a major
energetic investment and the number of eggs that females can produce in a
lifetime often limits female reproductive success. The reproductive
performance of a female is also dependent on her sexual partner in several
ways. In some species males contribute to reproduction directly, for example
by providing females with food and protection from predators and the sexual
harassment of other males, or by incubating the eggs and providing paternal
care to the young. In many other species a male’s only contribution to
reproduction is sperm; however, even in these species males can crucially
influence reproductive performance through the genes that the offspring
inherit from their father. Because males typically differ in the quality of
benefits which they convey to females, females can increase reproductive
success by carefully selecting partners and by copulating preferentially
with those males that are likely to convey the highest benefits.
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The idea that females could select sexual
partners was first suggested by Darwin in 1871 and was
initially encountered with much scepticism.
However, since then ample evidence has been gathered to indicate that
females have evolved many strategies to bias the probability of obtaining
sperm from individual males. In many species females are known to both: (1)
be attracted by a specific male stimulus or trait (Table 1); and (2) consistently
bias copulation success in favour of males whose
displays generate the strongest stimuli. This indicates convincingly that
in these species an important proportion of females does not copulate
randomly but selects sexual partners in a predictable way. Two studies of
the three-spined stickleback, Gasterosteus aculeatus
(Semler, 1971), and the long-tailed
widowbird, Euplectes progne (Andersson, 1982) provided the first
experimental demonstrations of female preference for certain male
phenotypes. Female sticklebacks prefer to lay their eggs in the
nests of males sporting red throats. The experimental manipulation of male
throat colour revealed the causal relationship
between the brightness of male throat and female reproductive decisions.
Male widowbirds have long tails that are used
during courtship displays. By manipulating tail length, Andersson
unequivocally demonstrated female preference for males sporting extremely
long tails. See also: Darwin, Charles Robert; Evolutionary ideas: Darwin
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Criteria of female choice
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The adaptive nature of female criteria of
partner choice is less clear. In species where males contribute directly to
reproduction through the provision of fitness-related commodities, females
are expected to select partners who are likely to convey the best benefits to
the current reproductive event or will make the best fathers.
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One obvious way through which males
directly contribute to reproduction is by providing sperm. Although males
generally produce many sperm relative to the number of eggs to be
fertilized, frequent copulation may deplete male sperm reserves (see below)
and females that copulate or obtain semen from sperm-depleted males may not
have enough sperm to fertilize all the eggs. Under these particular
circumstances mechanisms through which females can detect and select
against sperm-depleted males may evolve, for example through the avoidance
of males exhibiting phenotypic traits which signal depleted sperm reserves
(e.g. reduced courtship rate in some fish). However, there is little
evidence to suggest that the constraint imposed by sperm depletion on
female reproductive success is a widespread evolutionary force.
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In many cases, and especially in species
with little or no male contribution to reproduction, the evolution of
female preference may be explained by the genetic benefits that females
obtain by having their eggs fertilized by the preferred male type. This may
happen if: (1) male displays are costly to produce; (2) the attractiveness
of male displays covaries with male condition;
and (3) male condition is partly genetically determined. In this case
preferred males may be more likely to transmit alleles that convey superior
viability to the offspring. Moreover, female preference for a male display
determines the superior attractiveness and reproductive success of those
males which produce the best display. Provided that the differential
expression of male display is paternally heritable, females copulating with
the most attractive males may produce sons who will in turn experience high
reproductive success by inheriting genes for attractive displays from their
fathers. Although there is ample evidence suggesting that male displays are
costly and their quality is condition-dependent, the evidence that female
choice is based on genetic benefits is very limited. In the stalk-eyed fly,
Cyrtodiopsis dalmanni,
females prefer to copulate with males with longer eye span. Males tend to
develop longer eye span if they grow in a more benign environment and are
in better condition, indicating that developing this trait imposes a cost
to males. However, some genetic lines of males develop relatively long eye
span regardless of the quality of the environment where they are raised,
suggesting that some male genotypes consistently produce better sexual
displays than others and that eye span can be a reliable indicator of male
genetic quality (David et al., 2000). In
addition, in some fly populations some males carry X-chromosomal selfish
elements which destroy male spermatozoa (i.e. carrying the Y- rather than
the X-chromosome) through meiotic drive, thereby increasing the success of
the X-chromosome. The production of fewer viable male sperm reduces male
reproductive success because: (1) producing fewer sperm limits male
fertilizing efficiency, particularly in sperm competition; and (2)
producing fewer male sperm may translate into the production of a
suboptimal number of sons. Long male eye span appears to be genetically
linked to a region on the Y-chromosome that prevents meiotic drive;
therefore, females preferentially copulating with males sporting long eye
span may also increase their reproductive fitness through both the
production of an optimal number of male offspring, and through their
superior fertility (Wilkinson et al., 1998).
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Although there may be specific male
stimuli which are attractive to the majority of females, criteria of
partner choice may differ to some extent between females. One of the reasons
underlying variation in female choice of copulation partners is the fact
that under some circumstances it is the combination of a male and a female
rather than male quality alone that determines reproductive success. In
these cases females are expected to choose partners that are genetically
compatible or that complement female genomes, and not all females of a
population are expected to share a preference for a particular male or male
type. For example, the major histocompatibility
complex (MHC) is a set of genes that are involved in the coding of proteins
that allow T cells to identify foreign peptides and thus play a fundamental
role in vertebrate immune response regulation. MHC haplotypes
are typically highly polymorphic and differences between individuals may
underlie variation in parasite resistance and immune susceptibility between
individuals. Parents sharing the same MHC haplotypes
will produce offspring that are likely to have impaired immune response due
to MHC homozygote deficiency. Recent evidence suggests that females sharing
the same MHC haplotype with their copulation
partners experience reduced reproductive success due to impaired viability
of the young, and that females of several species tend to copulate
preferentially with males of a different MHC haplotype
than their own. MHC characterizes the body odour
of an individual and recent experimental tests suggest that females may use
body odour as a cue to assess the genetic
compatibility of potential partners. See also: Major histocompatibility
complex (MHC); Histocompatibility antigens
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A critical test of the hypothesis that
female choice of partner is beneficial to the female is to demonstrate that
females that are allowed to choose their copulation partners experience
higher total fitness (based on the lifetime reproductive success of a
female and the reproductive performance of her offspring) than females that
cannot choose with whom to copulate (i.e. copulate randomly). Despite the
inherent appeal of the idea that females increase their fitness by selecting
sexual partners, very few studies have clearly demonstrated this. While it
is difficult to carry out experiments to test the adaptive nature of female
choice of partners, it is useful to bear in mind that female choice for a
particular male type may not necessarily evolve because it is beneficial to
females. Males that are preferred by females may be more successful at
manipulating female choice (i.e. seducing females), without necessarily
delivering superior fitness benefits.
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Strategies of female choice
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How do females bias copulation success in favour of the preferred male type? In many species
females have considerable control over from whom they obtain sperm. Females
can actively select the best partner(s) by sampling the quality of the territories
of several males and assessing the expression of their sexual traits. They
can directly solicit sex from the most attractive male(s), and resist the
sexual advances of less attractive males. Females may favour
inseminations from favourite partners by
preferentially associating with these males and avoiding less attractive
males. Differential solicitation and resistance to sex can have a profound
influence on copulation success and can dramatically bias the probability
that a female will obtain sperm from a particular male. For example, in
some lekking species many females can queue to
copulate with a male, while avoiding males in adjacent territories, thus
dramatically skewing the copulation success of individual males.
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Indirect female choice
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Often males are larger than females,
socially dominant over females or simply too many: in such cases resisting
unwanted copulations can be a costly and risky business for females. When
females cannot efficiently avoid all unwanted copulations by direct resistance,
researchers have discovered that females are able to influence the outcome
of copulation in more subtle ways. For example, female feral fowl, Gallus
gallus domesticus,
show a marked preference for socially dominant copulation partners and
actively bias copulation success in favour of
high-ranking males. However, male fowl are larger and socially dominant
over females and direct resistance of unwanted copulation can result in
high costs to females and in limited success. Therefore, female fowl have
evolved more subtle strategies to favour
inseminations from dominant males. When resistance cannot prevent a
low-ranking male from copulating, a female utters a call which attracts the
attention of other males and incites competition between males over the
current copulation. The outcome of male–male competition is typically that
a male dominant over the copulating male disrupts the copulation and
sometimes inseminates the female. Thus, by manipulating male behaviour and
inciting competition over a copulation opportunity, female fowl reduce the
likelihood of an unwanted copulation and increase the probability of being
inseminated by preferred dominant males (Pizzari, 2001). Soliciting male–male
competition is a less costly way of biasing insemination success and may
also provide females with important clues as to the relative competitive
ability of males.
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Similarly, females may also avoid the
costs of sampling potential partners by adopting a ‘rule of thumb’ to
estimate male attractiveness (regardless of whether male attractiveness is
heritable, associated with a heritable condition, with compatible genes, or
not associated with any benefit to females). In species where there is
intense male–male competition for certain territories or displaying areas
the males which hold these territories are likely to be socially dominant
and/or in better condition than other males. Females may therefore avoid
the costs of selecting the best copulation partners by copulating with the
male(s) that own the best territories. In other species assessment of male
attractiveness may be more sophisticated and females may use a combination
of clues (e.g. position or quality of territory owned and display ability).
Another strategy that females may adopt to increase the probability of
copulating with the best males, and to reduce the costs associated with male
sampling (e.g. sexual harassment, time and energy invested in searching for
different males), is to copy the choice of other females. In some fish
species where females lay eggs in nest built and protected by a male, a
female is more likely to deposit eggs in nests where the eggs laid by other
females are visible.
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Female Polyandry
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The recent emphasis on female sexual
behaviour has revealed that females often actively seek copulations with
more than one male within a reproductive event. In addition, a number of
studies have shown that females can increase their reproductive success by
copulating with multiple males. Female reproductive success is mainly
limited by the number of eggs produced (see above) and thus is not expected
to increase with the degree of polyandry. Why this should be the case is
still unclear; many mechanisms that could explain the evolution of female
polyandry have been described (Table 2). In several
invertebrate species males transfer nutrients in their semen; therefore,
females that copulate more obtain more nutrients and this advantage often
translates to the production of more or better eggs. Similarly, a male may
help a female to care for her young if he is likely to be the father. In
the dunnock, Prunella
modularis, a small songbird, a female often
has two partners with whom she copulates at a frequency high enough to
allow both males to father at least some of the young. By copulating
frequently with two males, female dunnocks obtain
two helpers to raise their clutch (Davies, 1982). When there are
too few attractive males the competition to pair up with them may be too
intense. Under these circumstances females that form a social bond with a
less attractive male are then likely to seek copulations cryptically with
the most attractive males outside the social bond. These copulations are
referred to as extra-pair copulations and have been best studied in birds.
Many birds reproduce in monogamous pairs, in which both partners were
traditionally believed to be sexually faithful to each other and to
cooperate fully in raising a clutch successfully; however, recent studies
have shown that in most species these pair bonds are only social and that
both males and females can actively seek sexual encounters outside such
bonds. Female extra-pair copulation strategies are necessarily cryptic: the
pair male may discourage the promiscuity of his female with aggressive behaviours, or possibly by withdrawing paternal care
from a brood in which his paternity may be threatened by the sperm of
extra-pair males. One of the most striking examples of stealthy extra-pair
copulation strategies by female birds comes from a study of the Australian
superb fairy-wren, Malurus cyaneus. Radiotelemetry
of females revealed that when they are most fertile (i.e. when an
insemination is most likely to result in fertilization, 2–4 days before the
first egg is laid), females of this species undertake quick forays before
dawn, unseen by their social partners, to have extra-pair copulations with
males of distant territories (Double and Cockburn, 2000).
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