Postcopulatory sexual selection: Darwin’s omission and its consequences William G. Eberhard1 Smithsonian Tropical Research Institute and Escuela de Biologia, Universidad de Costa Rica, San Jose´, Costa Rica In one of his few major oversights, Darwin failed to appreciate that Table 1. Different types of competition among males for access male–male competition and sexual selection can continue even to conspecific females and their gametes (types of sexual after copulation has begun. The postcopulatory equivalents of selection) that occur before and after copulation both direct male–male battles (sperm competition) and female Time Intrasexual selection Intersexual selection choice (cryptic female choice) occur within the female’s body. Recognition of this hidden, but intense, sexual competition pro- Before copulation Male–male battles Classic female choice vides new insights into a variety of fields. These include the During and after Sperm competition Cryptic female choice hyperdiverse and paradoxically elaborate morphology of both copulation sperm and male genitalia, the equally puzzling and elaborate morphology of nongenitalic male structures that are specialized to grasp and stimulate females, powerful manipulative effects of have initiated copulation. Simply stated, Darwin missed the fact substances in male semen on female reproductive physiology, that not all copulations result in insemination, and that not all paradoxical male courtship behavior that occurs after copulation inseminations result in fertilization of the female’s eggs. Any has already begun, variability in parental investments, and the male ability to improve the chances that his copulations will lead puzzlingly complex and diverse interactions between sperm and to fertilizations of eggs will give him an advantage in competition female products that surround animal eggs and between male with other males who mate with the same female. gametophytes and female tissues in flowering plants. Many bizarre traits are involved, including male genitalia that are de- It was not until 99 years after Darwin’s 1871 book that Geoff signed to explode or fall apart during copulation leaving behind Parker (2) awakened evolutionary biologists to the evolutionary parts within the female, male genitalia that ‘‘sing’’ during copu- importance of processes that occur after the male has already lation, potent seminal products that invade the female’s body achieved genital coupling (conventionally called, somewhat im- cavity and her nervous system to influence her behavior, and a precisely, postcopulatory processes; they include processes dur- virtual Kama Sutra of courtship behavior performed after rather ing copulation). Parker saw that they, too, like the precopulatory than before genital coupling, including male–female dialogues events emphasized by Darwin, can result in sexual selection on during copulation. a male by affecting his success in competition with other males. There are postcopulatory equivalents inside the female of cryptic female choice ͉ sexually antagonistic coevolution Darwin’s precopulatory male–male struggles and female choice (Table 1). If a female copulates with Ͼ1 male, and if one of these icture a pile of freshly-cut weeds at the sunny edge of a males is better than others at, for instance, removing sperm Ptropical forest. Metallic green flies dart and circle over it, stored from previous males (3), this male will stand to sire more chasing one another in short dashes. Your eye is caught when a offspring and win out over the others. Appreciation that female chase ends as one fly grasps another in midair and the pair biases can also have postcopulatory effects on male reproductive immediately lands on the pile of weeds. Their genitalia are success, and thus exercise the postcopulatory equivalent of already coupled, and the male immediately turns to face away female choice among males, lagged behind (4, 5), and was not from the female. After a few seconds, paradoxically (because he presented as a general theory, however, until 1996 (6). After an is already securely attached), he begins to court, rhythmically initial period of negative reactions (7–9), CFC is now routinely waving his colorful hind legs and tapping the female’s abdomen. included as a possible factor in studies of possible postcopulatory The courtship continues for a few minutes as the pair remains sexual selection (10–12). Because important postcopulatory coupled, and then the flies separate. The female walks down into events are played out inside the female’s body, where she is the pile where she lays eggs (her larvae will feed on the rotting largely in control of what happens, female choice seems a priori vegetation), while the male rejoins the frenetic chases above more likely to be important after copulation than it is leading up the pile. to copulation. There is a surprisingly long list of female- Why would a male fly wait to court a female until after he has controlled processes that must be executed if insertion of the already achieved his evolutionary objective of copulating with male’s genitalia into the female is to result in siring her offspring her? The answer (recently worked out by a Brazilian graduate (Table 2). Other things being equal, any male better able to student, F. Barbosa, personal communication) had to wait for induce the female to carry out one of these processes more Ͼ100 years after Darwin’s great book on sexual selection (1) that explained so many other aspects of male–female sexual inter- completely than she does when mating with other males stands actions. to produce more offspring. The Puzzle of Darwin’s Omissions This paper results from the Arthur M. Sackler Colloquium of the National Academy of Darwin was uncannily on target about most of the topics he Sciences, ‘‘In the Light of Evolution III: Two Centuries of Darwin,’’ held January 16–17, 2009, discussed, and he seldom missed general phenomena that had at the Arnold and Mabel Beckman Center of the National Academies of Sciences and important consequences for his ideas. Strangely, however, there Engineering in Irvine, CA. The complete program and audio files of most presentations are ࿝ is a major missing piece in Darwin’s thinking on sexual selection. available on the NAS web site at www.nasonline.org/Sackler Darwin. He discussed at length how competition between males for Author contributions: W.G.E. wrote the paper. sexual access to females leads to sexual selection (1), but failed The author declares no conflict of interest. to realize that sexual selection [sperm competition and cryptic This article is a PNAS Direct Submission. female choice (CFC) in Table 1] can also occur even after males 1E-mail: [email protected]. www.pnas.org͞cgi͞doi͞10.1073͞pnas.0901217106 PNAS ͉ June 16, 2009 ͉ vol. 106 ͉ suppl. 1 ͉ 10025–10032 Downloaded by guest on September 27, 2021 Table 2. Female-controlled processes that occur in different sperm competition explains a number of hitherto paradoxical species and are known to increase the chances that a given observations. A male can dilute the sperm from previous males male will sire her offspring with his own voluminous ejaculate, engaging in what is called 1. Permit penetration deep enough to allow sperm deposition at the ‘‘raffle competition’’ (8). This tactic is apparently common in optimum site for storage or fertilization vertebrates, where testes size (and thus ejaculate size) correlates 2. Refrain from terminating copulation prematurely with the degree of female polyandry (13, 14). Behavioral traits 3. Transport sperm to storage and fertilization sites of males to prevail in sperm competition include transferring 4. Modify internal conditions (e.g. pH) inside reproductive tract to larger ejaculates when more males are in the vicinity (15) and reduce defenses against microbial invasion that kill sperm performing ‘‘retaliatory’’ copulations when the female with 5. Nourish or otherwise maintain sperm alive in storage site which a male is paired copulates with another male (14). 6. Refrain from discarding sperm from current male Another tactic involves the behavior and morphology of the 7. Discard sperm from previous male sperm themselves, with the sperm from a male linking together 8. Move sperm from previous male to site where current male can so that the group can swim more vigorously (16). The male can remove them also use his own genitalia or a spermatophore to physically 9. Accede to male manipulations that result in discharge of his displace sperm from previous males that are present in the spermatophore female (10, 17). Waage‘s classic study of sperm removal in a 10. Grow more immature eggs to maturity (vitellogenesis) damselfly (3) showed that during the first portion of copulation 11. Ovulate the female’s sperm storage organs (spermathecae) gradually 12. Produce eggs with more nutrients become depleted of sperm as the male moves his genitalia in and 13. Oviposit all available mature eggs out, snagging sperm on thick arrays of spines on his genitalia. 14. Prepare uterus for implantation Then after the spermathecae are nearly empty, the male ejac- 15. Refrain from removing copulatory plug produced by male ulates and fills them again with his own sperm. 16. Aid male in the formation of copulatory plug The male can also increase his chances of winning out in sperm 17. Modify morphology following first copulation to make competition by using defensive strategies, such as reducing the subsequent insemination more difficult danger of competition for his own sperm by guarding the female 18. Refrain from removing spermatophore before all sperm are from copulation with additional males (by staying with her after transferred copulation, physically plugging her genitalia, or inducing non- 19. Abort previously formed zygotes receptive behavior). Several other competitive mechanisms have 20. Refrain from aborting zygotes from current sperm been proposed, including ‘‘kamikaze’’ sperm that kill or disable 21. Allow germination of pollen grains the sperm of other males (18), and douche-like flushing out 22. Promote growth of pollen tubes and guide them toward ova stored sperm from the female with a jet of water (5), but they 23.