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Reproductive Social Behavior: Cooperative Games to Replace Sexual
Selection
Joan Roughgarden,* Meeko Oishi, Erol Akcay
*To whom correspondence should be addressed. E-mail: [email protected]
Published 17 February 2006, Science 311, 965 (2006)
DOI: 10.1126/science.1110105
This PDF file includes:
Table S1
References and Notes
Table 1 (Online) Critique of Sexual Selection Theory.
In: Reproductive Social Behavior: Cooperative Games
to Replace Sexual Selection
Joan Roughgarden,1∗ Meeko Oishi,2 Erol Akcay,1
1
Department of Biological Sciences, Stanford University,
2
Stanford CA 94305-5020, USA
Sandia National Laboratory, PO Box 5800
Albuquerque, NM 87185-1137, USA
∗
To whom correspondence should be addressed;
E-mail: [email protected].
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EMPIRICAL DEPARTURES
1.
Male/female binary for gametes, not bodies.
2.
Multiple male and female templates (genders) not uncommon.
3.
Sex-role reversal (coy males, passionate females) not uncommon.
4.
Sexual monomorphism not uncommon.
5.
Monogamy not uncommon.
6.
Sperm ejaculate size similar to egg size.
7.
Egg size evolutionarily plastic.
8.
Mating, including same-sex, often social.
THEORETICAL DIFFICULTIES
9.
Inconsistent with benefit to sexual reproduction.
10.
Maintaining bad genes impossible (paradox of lek).
11.
Different fitness definition for male and female incorrect.
12.
Traits hitchhike on female direct-benefit choices.
BEHAVIORAL DISCREPANCIES
13.
Females choose direct ecological, not indirect genetic benefits.
14.
Females rarely endorse victor of male combat.
15.
Secondary sex characters mostly for social inclusion.
16.
Deceit and incapacity not demonstrated.
17.
Insulting language subordinates nonconformity.
2
Table. 1. 1. Whole organisms, unlike gametes (small and large), do not obey near-universal binary division into male and female. 2. Multiple templates,“biological genders” (1) or alternative
life histories, often occur within each sex. 3. Sex roles often reverse relative to sexual-selection
prescriptions (drab males, showy females). Males and females may choose each other, “partial
sex-role reversal” (2). In sex role reversal, male parental investment exceeds females’ (3, 4).
Sex-role reversal inducible experimentally by manipulating resources available to each sex (5).
Describing sex-role reversal with parental-investment terminology does not explain phenomenon. Sex-role reversal shows total parental investment not determined by gamete size. 4.
Males and females often identical in external phenotype, lacking sexually-selected characters.
5. Males often not more promiscuous than females, and monogamy not uncommon (6) 6. Ejaculate of 106 sperm comparable to size of egg, implying equal initial investment of male and
female to zygote. 7. Egg size not evolutionarily constrained. Females vary egg size to determine brood size and time when offspring become self-supporting. 8. Mating often social, not
immediately procreative, and builds affiliative bonds among adults to protect and raise young.
Over 300 species of vertebrates naturally employ same-sex sexuality. (7) 9. Sexual selection
inconsistent with sexual reproduction’s function to share genes. Gene-sharing yields higher
between-generation geometric mean of within-generation arithmetic mean fitness compared to
clonal reproducers which face rapid extinction. (8) If gene-sharing were bad, those with best
genes would reproduce clonally, not dilute with others. Sexual selection teaches that powerful
males weed, and discerning females cleanse, bad genes from gene pool, culminating in species
betterment. Evidence rejects this hypothesis for spontaneous mutations. (9) 10. Sexual selection
requires intermediate heritability for secondary sexual characters, according to “paradox of the
lek.” If female choice for best secondary-sexual characters is intense, heritability should be low,
leaving no remaining basis for female choice. If females are indifferent to secondary-sex characters, heritability should be high, like characters not subject to directional selection. In fact,
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the heritability of sexually selected characters is high (about 0.6) (10) implying indifference
to rank-ordered genetic quality. Instead, females choose genetic complementarity—best match
not best male, or phenotypic state (health) (11). “Resolving” lek-paradox impossible. (12) 11.
Sexual selection incorrectly defines male fitness as “mating success” and female fitness as egg
number. Obviously, definition of fitness is identical for males and females: number of offspring
successfully reared. Asymmetrical definition produces war stories, whereas single definition invites negotiation-stories. Latest war story postulates females choose males who hurt them least.
Female choice enables male abuse: “females that suffer a direct fitness cost by mating with
the most coercive males receive compensation via the coerciveness of their sons” (13), so that
females “gain by losing.” (14) In experimental populations of Drosophila, seminal fluids from
mating male enter female’s blood, causing refusal to mate with subsequent males but lowering
female’s viability as side effect. (15) Data from insects and spiders do not support generality
to this story (16). If associating with males is dangerous enough, females can evolve asexual
reproduction. 80% of fruit-fly species have some all-female reproducing individuals and selection in laboratory yields vigorous all-female strain (17). 12. Genes hitchhike on mate choice
for direct benefits. Females should not transfer decision criterion, direct benefits, to less accurate genetic correlate of that benefit, allowing males to control information. 13. Female choice
usually observed for males resulting in direct benefits like infanticide avoidance, nest guarding,
and food provisioning; evidence for genetic benefits is scanty (18). Direct ecological benefits far larger than projected genetic benefits, making indirect genetic benefits moot. (19) 14.
Female choice does not always endorse victors of male-male combat. (20) 15. Secondary sexual characters may promote same-sex relationships rather than attract between-sex courtship.
Penis on female spotted hyenas and combs on male roosters may qualify animals to participate in same-sex groups that control opportunity to mate and rear young (“social inclusionary
traits”) (1). Balanced-design experiments to discern both within-sex and between-sex attractive4
ness of secondary-sexual characters lacking. 16. Behavior inconsistent with sexual-selection
written off as deceit or incapability. Same-sex sexuality excused as deception, or practice for
later heterosexuality. Feminine males condemned as “female mimics” who “steal” copulations
and sexually “parasitize” masculine males. Such social deceit never demonstrated, and implausible given imperfect resemblance of homosexual and feminine males to females, and extended
time during which highly visual animals socially examine each other. 17. Theoretical importance of social behavior contradicting sexual selection minimized through insulting vocabulary.
Primary scientific literature littered with “faithful” females vs. “promiscuous cheaters”, “cuckolded” males, “sneaker” males, “sneaky f—ers”, transvestite serpents, kleptoparasitic juveniles,
and legitimate vs. “illegitimate” nestlings. Demeaning nonconforming animals subordinates
them to sexual-selection narrative their existence falsifies.
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References and Notes
1. Roughgarden, Joan. 2004. Evolution’s Rainbow: Diversity, Gender and Sexuality in Nature
and People. University of California Press.
2. Bonduriansky, R. 2001. The evolution of male mate choice in insects: a synthesis of ideas
and evidence. Biol. Rev. 78:305–339.
3. Clutton-Brock, T. and A. C. J. Vincent. 1991. Sexual selection and the potential reproductive rates of males and females. Nature 351:58–60.
4. Emlen, S. T. and L. W. Oring. 1977. Ecology, sexual selection, and the evolution of mating
systems. Science 197:215–223.
5. Gwynne D. T. and L. W. Simmons. 1990. Experimental reversal of courtship roles in an
insect. Nature 346:173–174; Fosgren, Elizabet, Trond Amundsen, Asa A. Borg, and Jens
Bjelvenmark. 2004. Unusually dynamic sex roles in a fish. Nature 429:551–554.
6. Clutton-Brock, T. 1989. Review lecture: mammalian mating systems. Proc. Roy. Soc. London B. 236:339-372.
7. Bagemihl, B. 1999. Biological Exuberance St. Martin’s Press. New York.
8. Roughgarden, J., 1991. The evolution of sex. The American Naturalist, 138(4) pp. 934-985.
9. Radwan, J., Unrug, J., Snigórska, K. and Gawronska, K. (2004). Effectiveness of sexual
selection in preventing fitness deterioration in bulb mite populations under relaxed natural
selection. J. Evol. Biol., 17, 94-99; Radwan, Jacek 2004. Effectiveness of sexual selection
in removing mutations induced with ionizing radiation. Ecology Letters 7:1149–1154.
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10. Pomiankowski, A., and A. P. Møller. 1995. A Resolution of the lek paradox. Proc. Roy.
Soc. London. B. 260:21–29.
11. Gowaty PA, Drickamer LC, Schmid-Holmes S., 2003, Male house mice produce fewer
offspring with lower viability and poorer performance when mated with females they do
not prefer. Animal Behaviour 65:95–103; Coleman, Seth, Gail Patricelli, and Gerald Borgia, 2004, Variable female preferences drive complex male displays. Nature 428:742–745;
Apanius V, Penn D, Slev PR, Ruff LR, Potts WK, 1997, The nature of selection on the major
histocompatibility complex. Critical Reviews in Immunology 17:179–224; Neff, Bryan D.
and Pitcher, Trevor E., 2005, Genetic quality and sexual selection: an integrated framework
for good genes and compatible genes. Molecular Ecology 14:19–38.
12. Kirkpatrick, Mark and Michael Ryan. 1991. The evolution of mating preferences and the
paradox of the lek. Nature 350:33-38; Rowe, Locke, and David Houle. 1996. The lek paradox and the capture of genetic variance by condition-dependent traits. Proc. Roy. Soc. London. B. 263:1415–1421; Tomkins, Joseph L., Jacek Radwan, Janne S. Kotiaho, and Tom
Tregenza. 2004. Genic capture and resolving the lek paradox. Trends in Ecology and Evolution. 19:323-328.
13. Hosken, David and Rhonda Snook, 2005, How Important Is Sexual Conflict? Am. Nat.
165:S1-S4.
14. Eberhard, William G. 2005. Evolutionary Conflicts of Interest: Are Female Sexual Decisions Different? Am. Nat. 165:S19-S25.
15. Rice, W. R. 1996. Sexually antagonistic male adaptation triggered by experimental arrest
of female evolution. Nature 381:232234.
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16. Eberhard, W. G. 2004. Male-female conflict and genitalia: failure to confirm predictions in
insects and spiders. Biological Reviews 79:121186.
17. Carson, H. 1967, Selection for parthenogenesis in Drosophila mercatorium. Genetics,
55:157–171.
18. Hrdy, S. 1977. The Langurs of Abu: Male and Female Strategies of Reproduction. Harvard
University Press. Cambridge MA.
19. Moller AP, Jennions MD, 2001. How important are direct fitness benefits of sexual selection? Naturwissenschaften 88: 401–415.
20. Forsgren, E. 1997. Female sand gobies prefer good fathers over dominant males. Proc. Roy.
Soc. London B 264:1283–1286.
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