Behavioral Ecology Vol. 10 No. 4: 462-464
© 1999 International Society for Behavioral Ecology
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Female multiple mating, inbreeding avoidance, and fitness: it is not only the magnitude of costs and benefits that counts
Zoologisches Museum, Universität Zürich-Irchel, Winterthurerstr. 190, CH-8057, Switzerland
Received 19 May 1998; revised 16 October 1998; accepted 22 December 1998.
While males are expected to be promiscuous, the adaptive significance of
females copulating with multiple males is less clear. This is because male
reproductive success typically relates directly to the number of females
inseminated, whereas for females reproduction is usually unaffected by the
number of ejaculates received beyond one
(Bateman, 1948
;
Parker, 1992b;
Thornhill and Alcock, 1983).
Female multiple mating (defined here as females mating with multiple males)
may be male driven, but females often directly solicit copulations from a
number of males, and it is becoming increasingly clear that many (or most)
females in a wide range of taxa are genetically polyandrous
(Gowaty, 1994).
The benefits to females of such behavior may be direct, such as nutrients
or fertility insurance (e.g., Birkhead and
Fletcher, 1995; Sheldon,
1994; Simmons,
1992) or, alternatively, benefits may be genetic. Genetic benefit
arguments explaining female multiple mating typically relate to male quality
and may require females to be able to choose males with the desired
characteristic(s). Hypotheses include compensation for low-quality partners
(Kempenaers et al., 1992),
avoidance of genetic incompatibility (Zeh
and Zeh, 1996,
1997), promotion of sperm
competition (e.g., the intrinsic male quality hypothesis,
Birkhead et al., 1993; the
sexually selected sperm hypothesis, Keller
and Reeve, 1995), the increased heterozygosity hypothesis
(Brown, 1997; see also
Müller and
Ward, 1995), the genetic diversity-benefit hypothesis
(Tooby, 1982), and genetic
bet-hedging (Watson,
1991).
Another possible benefit of multiple mating by females relates to avoiding
costs of inbreeding (Stockley et al.,
1993). Although Williams
(1975) argued multiple mating
produces little more offspring diversity than copulating with a single male,
this need not be true (Yasui,
1998). For example, models of hymenopteran offspring relatedness
and number of mating partners suggest offspring heterogeneity increases
steeply when the number of partners increases from one to five and sperm use
is random (Page and Metcalf,
1982; see also Yasui,
1998). Moreover, empirical data indicate that multiple mating can
potentially increase fitness in at least some instances (e.g.,
Liersch and Schmid-Hempel,
1998; and see Page and
Metcalf, 1982). For example, in bumble bee colonies increasing
within-colony genetic heterogeneity led to decreased parasite prevalence,
diversity and intensity (Liersch and
Schmid-Hempel, 1998). The authors proposed that genetic polyandry
(or polygyny) could therefore potentially increase fitness under parasitism
(Liersch and Schmid-Hempel,
1998), and this has recently been confirmed
(Baer and Schmid-Hempel, 1999).
It has also been proposed that female multiple mating reduces the fitness
cost(s) of inbreeding in some instances
(Stockley et al., 1993), a
hypothesis that has been widely discussed (e.g.
Watson, 1997;
Zeh and Zeh, 1996). The
original argument was that if females cannot recognize or cannot avoid
copulating with close relatives, especially when dispersal is low, then female
multiple mating could increase female fitness by increasing the probability of
producing some outbred young (Stockley et
al., 1993), and it is the inbreeding avoidance hypothesis that we
consider here.
It is clear that outbreeding can be beneficial in fitness terms (e.g.,
Bateson, 1983;
Munson et al., 1996), and
Liersch and Schmid-Hempel's
(1998) bumble bee study
clearly indicated that, in terms of parasitism, females benefited from
producing genetically diverse offspring. However, in most species female
bumble bees typically copulate only once (and polygyny is uncommon) and the
question posed was why are females not copulating more frequently, as there
are clear fitness benefits (Liersch and
Schmid-Hempel, 1998). Obviously, there can be costs involved in
mating multiply (e.g., Thornhill and
Alcock, 1983) and, equally obviously, the relative magnitude of
the costs and benefits will influence selection for or against female multiple
mating and increased offspring heterogeneity. However, what is not intuitively
clear is that potential fitness benefits obtained by females from multiple
mating is crucially dependent on the shape of the relationship between
relatedness of copulatory partners and fitness. Explicitly, we argue here that
the overall relationship between partner relatedness or number and fitness can
be positive, but increased variance (i.e., more mates) may nonetheless be
selected against.
Functions relating fitness to other variables are typically thought to
adopt one of three shapes: linear, increasing with diminishing returns, or
sigmoid (e.g., Ricklefs,
1979). However, functions relating a character to fitness are
unlikely to be linear (e.g., Page,
1980; Ricklefs,
1979; Schmid-Hempel,
1994). Because the relationship between female fitness and number
of mates is typically unknown (because of the inherent problems of measuring
costs and benefits in fitness terms) but unlikely to be linear (see above), we
consider here the effect of multiple mating on fitness when this relationship
is either increasing and convex (i.e., f'' > 0) or increasing
with diminishing returns (increasing and concave; i.e., f'' <
0).
Consider the relationship between fitness and relatedness of copulatory
partners, and note that inbreeding (high relatedness) is typically associated
with low fitness (e.g., Wildt et al.,
1987). A relationship where fitness benefits asymptotically
decrease (i.e., to the right of the point of inflection on our sigmoid curve,
Figure 1) would be expected
when there is a trade-off between costs (e.g., mate searching) and benefits
(see, e.g., Parker, 1992a).
Under these conditions random female mating with multiple males will not
increase fitness relative to singly copulating females, in spite of the
overall positive relationship between fitness and relatedness: a female with
less variation in the relatedness of her mates will have a higher average
fitness than a female with greater variance in mate relatedness [from
Figure 1; female A (with little
variation in mate relatedness) = solid lines, mean fitness = y,
compared with female B (large variation in mate relatedness) = dashed lines,
mean fitness = y — d]. Note that mean partner
relatedness is the same for both females, as expected if females cannot
distinguish between kin and nonkin (i.e., there is a equal chance of the next
partner being more or less related).
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Conversely, if the fitness function is exponentially increasing (i.e., to
the left of the point of inflection on our sigmoid curve,
Figure 1), as may occur when a
population is expanding into new habitat, females inseminated by few males
have a mean fitness of y (Figure
1; female C = solid lines), while females mating with many males
has a mean fitness of y + d
(Figure 1; female D = dashed
lines). (Note: if the relationship between fitness and relatedness is linear,
then multiple mating will not alter fitness relative to that of more
monogamous females, but see above.) The underlying assumption is that
variation on the x-axis (relatedness at insemination) is translated
into variation in fitness via genetic variation in the offspring and that
females mate nonselectively. When this occurs it is clear that the fitness
outcome of multiple mating will be influenced by the shape of the fitness
curve (convex or concave), or by a female's location on the x-axis
relative to the point of inflection when the curve is sigmoid
(Figure 1). For example, if a
female is closely related to her previous mating partner compared to the
general population (i.e., to the left of the point of inflection), she would
probably benefit from more random mating, and vice versa. The essence of this
argument has been applied in several other biological contexts (e.g.,
Parker, 1984;
Sherman et al., 1988),
including risk-sensitive foraging (e.g.,
Caraco et al., 1980), insect
growth under variable temperature (e.g.,
Blanckenhorn, 1997), and
Gillespie's (1977) classic
variance reduction principle.
Although the exact relationship between fitness and relatedness of mating
partners is often unknown, the curve(s) described above is a versatile
estimator covering a range of possibilities
(Page, 1980), and changing the
slope while retaining the shape of the curve(s) only alters the magnitude of
the results. We have shown that for multiple copulations to increase female
fitness, without pre- or postcopulatory selection and when mating is more or
less random (i.e., females cannot detect/choose high-quality males which by
definition increase female fitness; e.g.,
Petrie, 1994;
Welch et al., 1998; see also
Bateson, 1983), the
relationship between fitness and multiple mating must be convex and
increasing. However, note that because fitness obviously has an asymptote, the
convex relationship would typically be found to the left of the inflection
point of a logistic curve. Of course, if some pre- or postcopulatory selective
mechanism is operating, then the potential for fitness benefits increases.
This is true even when fitness is increasing with diminishing returns relative
to relatedness, as long as mean relatedness is shifted far enough to the right
to compensate for the decreased mean fitness generated by the increased
variation. This could be achieved by mate choice (e.g.,
Petrie, 1994), selecting
against self/like-self sperm, a process described in ascidians, lizards, and
many plants (e.g., Bishop,
1996; Olsson et al.,
1996; Willson,
1990), or if the competitive ability of sperm is greater in
outbred males (e.g., Wildt et al.,
1987). In addition, it has been argued that increased offspring
diversity may be favored even when it decreases mean offspring fitness (i.e.,
genetic bet hedging; Phillipi and Seger,
1989). However, it appears the evolution of female multiple mating
via the genetic bet hedging mechanism alone is highly unlikely
(Yasui, 1998; see also
Birkhead and Møller,
1992).
Returning to the shrew study above and the relationships between fitness
and genetic relatedness considered here, for Stockley et al.'s
(1993) hypothesis regarding
shrews to be accurate, the relationship of fitness to relatedness must be
increasing and convex, or there must be some postcopulatory influence(s) on
paternity. Note however in the latter case, there is no overt indication of
sperm selection by female shrews
(Stockley, 1997).
In conclusion, although it is intuitively clear that the magnitude of the costs and benefits of multimale copulations will influence selection for or against female multiple mating, the function relating female multiple mating to fitness will also have an effect. In spite of a positive relationship between fitness and female multiple mating, increased mate/offspring diversity can still be detrimental and therefore selected against under conditions that may be quite common in nature. Moreover, with all else being equal, we would expect female promiscuity to be more prevalent in species likely to face an increasing and convex fitness curve, such as those with high baseline costs of reproduction but negligible cost changes thereafter and/or those exhibiting semelparity. Although mate choice can increase fitness regardless of the fitness function, random multiple mating may also have fitness advantages under some conditions.
ACKNOWLEDGEMENTS
We thank Max Reuter, François Balloux, Paul Ward, Bart Kempenaers, Leigh Simmons, Paul Schmid-Hempel, Georgina Bernasconi, Paula Stockley, Fredrik Widemo, and the anonymous referees for comments and discussion. This work was supported by grants from the Swiss National Science Foundation.
REFERENCES
Baer B, Schmid-Hempel P, 1999. Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee.Nature 397:151-154.
Bateman AJ, 1948. Intra-sexual selection in Drosophila. Heredity 2:349 -368.[Web of Science][Medline]
Bateson P, 1983. Mate choice. London: Cambridge University Press.
Birkhead TR, Fletcher F, 1995. Male phenotype and ejaculate quality in the zebra finch Taeniopygia guttata. Proc R Soc Lond B 262:329-334.[Medline]
Birkhead TR, Møller AP, 1992. Sperm competition in birds: evolutionary causes and consequences. London: Academic Press.
Birkhead TR, Møller AP, Sutherland WJ, 1993. Why do females make it so difficult for males to fertilize their eggs?J Theor Biol 161:51-60.
Bishop JD, 1996. Female control of paternity in the
internally fertilizing compound ascidian Diplosoma listerianum. I.
Autoradiographic investigation of sperm movements in the female reproductive
tract. Proc R Soc Lond B
263:369-376.
Blanckenhorn WU, 1997. Effects of temperature on growth, development and diapause in the yellow dung fly—against all the rules? Oecologia 111:318-324.[Web of Science]
Brown JL, 1997. A theory of mate choice based on
heterozygosity. Behav Ecol
8:60-65.
Caraco T, Martindale S, Whittam TS, 1980, An empirical demonstration of risk-sensitive foraging preferences. Anim Behav 28:820-830.[Web of Science]
Gillespie JH, 1977. Natural selection for variance in offpspring numbers: a new evolutionary principle. Am Nat 111:1010-1014.[Web of Science]
Gowaty PA, 1994. Architects of sperm competition.Trends Ecol Evol 9:160-162.
Keller L, Reeve HK, 1995. Why do females mate with multiple males? The sexually selected sperm hypothesis. Adv Stud Behav 24:291-315.
Kempenaers B, Verheyen GR, Van den Broeck M, Burke T, Van Broekhoven C, Dhont AA, 1992. Extra-pair paternity results from female preference for high quality males in the blue tit.Nature 357:494-496.
Liersch S, Schmid-Hempel P, 1998. Genetic variation
within social insect colonies reduce parasite load. Proc R Soc Lond
B
265:221-225.
Müller G, Ward PI, 1995. Parasitism and heterozygosity influence the secondary sexual characters of the European minnow. Phoxinus phoxinus (L.) (Cyprinidae).Ethology 100:309-319.[Web of Science]
Munson L, Brown JL, Bush M, Packer C, Janssen D, Reiziss SM, Wildt
DE, 1996. Genetic diversity affects testicular morphology in
free-ranging lions (Panthera leo) of the Serengeti Plains and
Ngorongoro Crater. J Reprod Fertil
108:11-15.
Olsson M, Shine R, Madsen T, Gullberg A, Tegelström H, 1996. Sperm selection by females. Nature 383:585.
Page RE, 1980. The evolution of multiple mating
behavior by honey bee queens (Apis melifer L.).Genetics
96:263-273.
Page RE, Metcalf RA, 1982. Multiple mating, sperm utilization, and social evolution. Am Nat 119:263-281.[Web of Science]
Parker GA, 1984. Sperm competition and the evolution of animal mating strategies. In: Sperm competition and the evolution of animal mating systems (RL Smith, ed). London: Academic Press;2 -60.
Parker GA, 1992a. Marginal value theorem with exploitation time costs: diet, sperm reserves, and optimal copula duration in dung flies. Am Nat 139:1237-1256.[Web of Science]
Parker GA, 1992b. Snakes and female sexuality.Nature 355:395-396.
Petrie M, 1994. Improved growth and survival of offspring of peacocks with more elaborate trains. Nature 371:290-291.
Philippi T, Seger D, 1989. Hedging ones evolutionary bets, revisited. Trends Ecol Evol 4:41-44.
Ricklefs RE, 1979. Ecology, 2nd ed. New York: Chiron Press.
Schmid-Hempel P, 1994. Infection and colony variability in social insects. Phil Trans R Soc Lond B 346:313-321.
Sheldon BC, 1994. Male phenotype, fertility, and the
pursuit of extrapair copulations by female birds. Proc R Soc Lond
B
257:25-30.
Sherman PW, Seeley TD, Reeve HK, 1988. Parasites, pathogens, and polyandry in social Hymenoptera. Am Nat 131:602-610.[Web of Science]
Simmons LW, 1992. Quantification of role reversal in relative parental investment in a bush cricket. Nature 358:61-63.
Stockley P, 1997. No evidence of sperm selection by female common shrews. Proc R Soc Lond B 264:1497-1500.[Medline]
Stockley P, Searle J B, Macdonal, DW, Jones CS, 1993. Female multiple mating behaviour in the common shrew as a strategy to reduce inbreeding. Proc R Soc Lond B 254:173-179.[Medline]
Thornhill R, Alcock J, 1983. The evolution of insect mating systems. Cambridge, Massachusetts: Harvard University Press.
Tooby J, 1982. Pathogens, polymorphisms, and the evolution of sex. J Theor Biol 97:557-576.[Web of Science][Medline]
Watson PJ, 1991. Multiple paternity as genetic bet-hedging in female sierra dome spiders, Linyphia litigiosa.Anim Behav 41:343-360.[Web of Science]
Watson PJ, 1997. Multi-male mating and female choice increase offspring growth in the spider Neriene litigiosa (Linyphidae). Anim Behav 55:387-403.
Welch AM, Semlitsch RD, Gerhardt HC, 1998. Call
duration as an indicator of genetic quality in male gray tree frogs.Science
280:1928-1930.
Wildt DE, Bush M, Goodrowe KL, Paker C, Pusey AE, Brown JL, Joslin P, O'Brien SJ, 1987. Reproductive and genetic consequences of founding isolated lion populations. Nature 329:328-331.
Williams GC, 1975. Sex and evolution. Princeton, New Jersey: Princeton University Press.
Willson MF, 1990. Sexual selection in plants and animals. Trends Ecol Evol 5:210-214.
Yasui Y, 1998. The `genetic benefits' of multiple mating reconsidered. Trends Ecol Evol 13:246-250.
Zeh JA, Zeh DW, 1996. The evolution of polyandry. I.
Intragenomic conflict and genetic incompatibility. Proc R Soc Lond
B
263:1711-1717.
Zeh JA, Zeh DW, 1997. The evolution of polyandry. II.
Post-copulatory defence against genetic incompatibility. Proc R Soc
Lond B
264:69-75.
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