Nature's Nether Regions

by Menno Schilthuizen

  67 The female reproductive morphology for several species of sheet web spiders is described in, for example, Hormiga and Scharff (2005) and for the golden hamster in Yanagimachi and Chang (1963).

  68 The work on Neriene litigiosa is described in, for example, Watson (1991, 1995) and Watson and Lighton (1994), as well as in Eberhard (1996). Further details are based on an e-mail from Paul Watson of October 28, 2012. In reality, sierra dome spiders do not very often opt out by departing after the dry phase of copulation, instead relying more on sperm dumping in most cases.

  73 For the positive effects of proper female stimulation in artificial insemination, see Evans and McKenna (1986) and Eberhard (1991). Many more eyewitness accounts on artificial insemination in pigs are in Roach (2008).

  73 The work on the spotted cucumber beetle is in Tallamy et al. (2001).

  73 I took most of the information on the anatomy of the human clitoris and the history of its study from O’Connell et al. (1998, 2005) and Foldes and Buisson (2009). Particular details on Reinier de Graaf were taken from Rozendaal (2006), while the New Scientist article is Williamson (1998).

  74 The dissections of the clitoris by Kobelt are described in Kobelt (1844).

  75 My brief paragraph on the changing views on human female orgasm is largely based on Gould (1991) and Symons (1979). Freud’s ideas on female orgasm are in the third of his Three Essays on the Theory of Sexuality (Freud, 1905). The quote from The Naked Ape is from Morris (1967).

  76 The development of marsupial genitals is taken from Butler et al. (1999).

  76 Information on clitoris shape in several mammals was taken from Porto et al. (2010), Place and Glickman (2004), Rubenstein et al. (2003), and Bassett (1961).

  77 The quote by Tim Birkhead is from his Tinbergen Lecture at Leiden University on May 11, 2012.

  77 For the physiology of vaginal and clitoral orgasms, see Masters and Johnson (1966) and Gruenwald et al. (2007).

  77 The release of oxytocin during orgasm is from Blaicher et al. (1999).

  77 Information on brain regions activated during orgasm is from Georgiadis (2011).

  77 The urethrogenital reflex in female rats is described in, for example, Marson et al. (2003) and Giraldi et al. (2004).

  77 The reference for the work on pressure changes in the uteri of cows during copulation is VanDemark and Hays (1952).

  78 For female orgasm in primates, see Burton (1971), Hanby and Brown (1974), Symons (1979), Puts et al. (2012a), and Troisi and Carosi (1998).

  78 Other upsuck experiments on mammals, even nineteenth-century ones, can be found in Roach (2008). The references used for the bit about the upsuck hypothesis are Fox et al. (1970) and Baker and Bellis (1993b).

  80 The studies that used questionnaires to look for the effects of male attractiveness and penis length on orgasm frequency are Puts et al. (2012b) and Costa et al. (2012).

  80 The by-product hypothesis of the female orgasm is first coined in Symons (1979). The 0.8-second interval in both male and female orgasmic spasms is from Masters and Johnson (1966). Gould’s “clitoral ripples” essay is included in Gould (1991), and other recent publications in favor of the by-product hypothesis are Lloyd (2005) and Wallen and Lloyd (2008). See also Lloyd’s 2012 lecture at the Istituto Veneto, available at www.youtube.com/watch?v=m6GMeeOFUsE. Rebuttals of the by-product theory are in, for instance, Judson (2005), Hosken (2008), Lynch (2008), Zietsch and Santtila (2011), and Puts et al. (2012a).

  81 The role of oxytocin in sperm transport is in Wildt et al. (1998).

  81 I got the number of titles on the biology of the female orgasm in the years 2008–2012 by searching for “female orgasm” AND “biology” in Google Scholar.

  82 One story of a woman impregnating herself with her ex-husband’s sperm appeared in the UK’s Daily Mail on September 24, 2012.

  82 Lists of sperm longevity in various kinds of vertebrate animals are to be found in Birkhead and Møller (1993) and Holt and Lloyd (2010), and for social insects I used Boomsma et al. (2005).

  83 Eberhard (1996) lists a number of different sperm storage organs in female animals, including snakes, and Pitnick et al. (1999) give background information for flies and other insects. For snails, I used Baur (2007, 2010) and Evanno and Madec (2007), and for turtles, Gist and Jones (1989).

  84 For the story about the yellow dung fly, I primarily used Parker (2001), from which also Parker’s quotes are taken, Ward (1993), Hellriegel and Bernasconi (2000), Jann et al. (2000), Sbilordo et al. (2009), and Bussière et al. (2010).

  87 The Bruce effect was described by Bruce (1959, 1960). The examples from the Bruce effect in various vole species I took from Eberhard (1996: 164). The study on the Bruce effect in wild geladas is Roberts et al. (2012), while I also used Yong (2012).

  88 The information on natural abortion rates in humans is from Forbes (1997), Reeder (2003), and Wasser and Isenberg (1986), while the correlation between abortion and immune system similarity is in Knapp et al. (1996) and Ober et al. (1998) for macaques and humans, respectively. The reference to antiabortionists refers to the remarks by U.S. Senate candidate Todd Akin that “the female body has ways to try to shut that whole thing down.”

  Chapter 5: A Fickle Sculptor

  90 I took general ideas on sexual selection from Kuijper et al. (2012).

  90 The opening sentence quoted (“Let t be a male trait used by females in mate choice and p be the strength of female preference”) is from Iwasa and Pomiankowski (1995).

  90 I took some general information on stalk-eyed flies from Cotton et al. (2010) and from interviews with Hans and Cobi Feijen during the Kinabalu/Crocker Range Expedition, September 2012.

  91 The field trip with A. Pomiankowski and S. Sutton took place on April 17, 2006.

  93 The rare-male effect is described in, for example, Partridge (1988) and Kokko et al. (2007).

  93 The guppy experiments, from Hughes et al. (1999), were more complex (involving also a third, more variable group of males) than I have described them here, but by focusing only on the M1 and M7 males I hope I have represented their essence. The part of this section that deals with guppies was kindly checked by Michael Jennions.

  94 The haiku by Hanna Kokko is one that I took from her home page, biology.anu.edu.au/hosted_sites/kokko/Publ/index.html (and I apologize to her for not displaying it in proper three-line format).

  94 Her computer modeling of the rare-male effect is in Kokko et al. (2007). I made use of a lecture by and an interview with her in Leiden, February 15, 2013, and of comments she made after proofreading this section.

  95 The rapid change in Galápagos finches and other contemporary evolution is described in, for example, Weiner (1994).

  96 The book on the paleontology of sex is Long (2012).

  96 The fossilized turtle copulation is from Joyce et al. (2012), and the reproduction in extinct placoderms is in Long et al. (2008, 2009).

  96 The history of amber insect collections is in Poinar (1992).

  96 The synchrotron X-ray tomographic technique, as well as some results in imaging the genitalia of Baltic amber beetles, is in Perreau and Tafforeau (2011) and Perreau (2012). Michel Perreau read and checked the paragraphs on his work.

  97 The use of beetle fossils from peat and other Pleistocene and Holocene deposits is advocated by Coope (1979, 2004) and Schafstall (2012), and its history was clarified to me by Richard Preece during a meeting at Cambridge, UK, April 17, 2013. Coope and Angus (1975) give illustrations showing the excellent preservation of genitalia in such fossils, and the quotation is from Coope (2004).

  98 The original punctuated equilibria article is Eldredge and Gould (1972), whereas the terms “evolution by jerks” and “evolution by creeps” are mentioned in, for example, Jones (2008).

  99 The Darwin quote is from The Origin of Species (Darwin, 1859).

  99 The work on 3-D analysis of
clasper shape evolution in damselflies can be found in McPeek et al. (2008, 2009) and Shen et al. (2009).

  100 The studies that show jerky evolution in the genitals of flies and millipedes are, respectively, Richmond et al. (2012) and Wojcieszek and Simmons (2011).

  100 One of the citations that seem to have been the basis for the “size doesn’t matter” statement is Masters and Johnson (1966: 91).

  101 General background information on allometry is to be found in Klingenberg (1996).

  101 Surveys of negative allometry in the genitalia of large numbers of animal species are provided by Eberhard et al. (1998) and Eberhard (2008), whereas the stag beetle example is in Tatsuta et al. (2001). Retief et al. (2013), however, suggest that positive allometry may be common in mammal genitalia.

  102 The study of human penis length and shoe size is Shah and Christopher (2002), and the online survey is by Richard Edwards (www.sizesurvey.com).

  104 Allometry in guppy genitalia is mentioned in Eberhard (2008) and Kelly et al. (2000).

  104 The work on mosquito fish is in Langerhans et al. (2005) and in Kahn et al. (2010). The part of this section that deals with poeciliid fish was kindly checked by Michael Jennions.

  105 Background information on Tidarren was taken from Knoflach and Van Harten (2000). The term “one-shot genital apparatus” is from Schneider and Michalik (2011). The evidence that the Tidarren testes wither before maturation are from Michalik et al. (2010). The experiments on mobility are in Ramos et al. (2004). What I wrote on Tidarren was read by Peter Michalik, except the sentence on the evolution of small males and large females in this genus, which was added afterward and was taken from Hormiga et al. (2000).

  Chapter 6: Bateman Returns

  109 The functioning of the genitalia in damselflies is from Waage (1979), Córdoba-Aguilar et al. (2003), and Cordero-Rivera and Córdoba-Aguilar (2010).

  110 The details on Waage’s career are from an e-mail correspondence I had with him on March 14, 2013, and from his CV available from his home page at Brown University.

  113 Waage’s work on the spreadwing L. vigilax is in Waage (1982).

  113 The information on Calopteryx xanthostoma is from Siva-Jothy and Hooper (1996), and on Calopteryx haemorrhoidalis from Córdoba-Aguilar (1999, 2002).

  114 Sperm dumping in damselflies is discussed in Eberhard (1996).

  115 The quote on swords and shields is from Dawkins and Krebs (1979).

  115 The risks of anthropomorphizing sexual conflict and choosing a human-gender-associated terminology are discussed in Karlsson Green and Madjidian (2011).

  116 The experiments with artificial human genitals are in Gallup et al. (2003), whereas the results of their college student interviews are in Gallup et al. (2006).

  116 More information on the frequency of sexual encounters in women is in Baker and Bellis (1995).

  117 The data on single- or multi-perpetrator rape are, for example, in Vetten and Haffejee (2005).

  117 The information on chimpanzee promiscuity is in Tutin (1979).

  118 The Belgian-British fertilization-by-proxy article is Haubruge et al. (1999).

  118 I obtained basic information on shark genitalia and copulation from Gilbert and Heath (1972), Fitzpatrick et al. (2012), and Eilperin (2012).

  119 Whitney et al. (2004) published observations that they claim refute the sperm-flushing hypothesis for sharks, but I am not entirely convinced by their argumentation, which is why I have still decided to include sharks (with some caution) in the list of animals that do sperm displacement.

  119 Sperm removal in crickets and katydids is in Von Helversen and Von Helversen (1991), Ono et al. (1989), and Eberhard (1996).

  121 I thank Theo Schmitt for making me more fully aware of the genitalia of Aleochara. For the section on this genus, I used Gack and Peschke (1994, 2005) and Putnam (1988). Claudia Gack read and approved the text. I recommend Godfray (1994) for general information on insect parasitoids.

  125 The details of the act of homosexual necrophilia were taken from Moeliker (2001, 2009); Kees Moeliker also read and approved the text.

  125 The papers by McCracken on the Argentine lake duck are McCracken (2000) and McCracken et al. (2001), whereas the quotes by Birkhead are from his Tinbergen Lecture in Leiden, May 11, 2012.

  127 The information on penis pecking associated with duck mating on land is in Birkhead (2008: 313, 385).

  127 The work by Patricia Brennan is in Brennan et al. (2007, 2009). The section in which the work by Birkhead and Brennan is mentioned was checked by Tim Birkhead. Parts of this paragraph are based on a Dutch-language article I wrote in Bionieuws (Schilthuizen, 2010).

  128 Lange et al. (2013) is a general source of information on traumatic insemination.

  128 The copulation in Harpactea sadistica is described in Řezáč (2009).

  130 As a general source on bedbug reproduction I used Reinhardt and Siva-Jothy (2007). The quotes by Siva-Jothy are from his lecture at the Congress of the European Society for Evolutionary Biology, in Tübingen, Germany, August 20–24, 2011. Rivnay (1933) described how males detect moving females. The story that male bedbugs sometimes inseminate other males is in Lloyd (1979), but is considered not plausible by Judson (2002). Mellanby (1939) describes how females die after being housed with twelve males at the same time. The reduced life span caused by copulation is in Stutt and Siva-Jothy (2001). The experiments with replica bedbug penises are, for example, in Morrow and Arnqvist (2003).

  133 The sperm found in the blood of mites was mentioned to me by Gerd Alberti and Antonella di Palma during an interview in Greifswald, Germany, on December 18, 2012; it is also in Alberti (2002).

  133 The information on insemination of birds and mammals by injection of sperm is in Rowlands (1957).

  133 The study of pregnancy in women with noncommunicating uterine horns is Nahum et al. (2004).

  Chapter 7: Future Suitors

  135 My visit to Greifswald’s Zoological Institute and the interviews with Gerd Alberti, Antonella di Palma, Gabriele Uhl, Martin Haase, Peter Michalik, and Theo Schmitt took place December 17–19, 2012.

  135 Basic details on the reproduction of spiders and mites are in Alberti (2002), Alberti and Coons (1999), and Alberti and Michalik (2004). The piece of text on my interview with Alberti and Di Palma was read and approved by the former.

  136 An overview of mating plugs in spiders is in Uhl et al. (2010).

  136 The whole text on mating plugs in spiders was read and approved by Gabriele Uhl.

  137 The spread of the wasp spider is recorded in Kumschick et al. (2011), whereas the mating plug work in this species is in Nessler et al. (2007) and Uhl et al. (2007).

  139 The Tidarren work is in Knoflach and Van Harten (2001), Knoflach and Benjamin (2003), and Michalik et al. (2010).

  140 The first observation of a mating plug in a guinea pig is in Leuckart (1847; fide Dean, 2013), and in a chimpanzee in Tinklepaugh (1930).

  140 I obtained information on mating plugs in mammals primarily from Kingan et al. (2003), Carnahan and Jensen-Seaman (2008), Tauber et al. (1975), Hernández-Lopez et al. (2008), Dean (2013), Murer et al. (2001), Koprowski (1992), and Dixson and Anderson (2002). I wrote about Kingan’s work earlier (Schilthuizen, 2003).

  145 Information on women’s allergic reaction to semen is to be found at seminalplasmaallergy.org.

  145 I got the information on the numbers of proteins in Drosophila ejaculate from Findlay et al. (2008) and in human ejaculate from Pilch and Mann (2006).

  146 The quote by Rama Singh was taken from a lecture he gave at the ICSEB conference in Budapest, 1996; a recent paper by his group on this subject is Haerty et al. (2007).

  146 The way the Drosophila sex peptide works is summarized in, for example, Eberhard (1996), Gillott (2003), and Liu and Kubli (2003).

  147 The mode of action of semen proteins in other
insects was taken from Gillott (2003) and Eberhard (1996). Specifically, the studies on fire beetles, corn earworm moths, and ticks are in Eisner et al. (1996), Kingan et al. (1995), and Leahy and Galun (1972), respectively.

  147 Gallup et al. (2002) studied the possible psychological effects of semen in female college students.

  148 An overview of the relationship between semen and preeclampsia is in Robertson et al. (2003).

  148 The grasshopper experiments are from Hartmann and Loher (1999).

  148 The effects of seminal proteins on the female housefly are in Leopold et al. (1971) and Riemann and Thorson (1969).

  149 The two studies on banana fly semen that I mention are Chapman et al. (1995) and Civetta and Clark (2000).

  149 The seed beetle semen is discussed in Eady et al. (2007) and Yamane and Miyatake (2012).

  150 The paper on spiny longhorn beetle genitalia is Hubweber and Schmitt (2010).

  151 Overviews of spiny penises across the animal kingdom are in Eberhard (1985) and Cordero and Miller (2012); the latter paper is also the source for the caltrop cornuti in moths. The penile spines of hoary bats can be admired in Cryan et al. (2012).

  152 I talked with Göran Arnqvist on January 18, 2013, at the Linnaeusborg, University of Groningen, for the occasion of Bram Kuijper’s Ph.D. defense.

  152 The article in Nature is Crudgington and Siva-Jothy (2000).

  153 The postmating harm inflicted by Arnqvist and colleagues is described in Morrow et al. (2003).

  154 The microlaser experiments are in Hotzy et al. (2012).

  154 Other work on seed beetles by Arnqvist’s team is Rönn et al. (2007) and Hotzy and Arnqvist (2009).

  154 I spoke with Michal Polak about his experimental setup (see Polak and Rashed, 2010) after his lecture at the Congress of the European Society for Evolutionary Biology in Tübingen, Germany, August 20–24, 2011.

  154 General information on primate penis spines is from Zarrow and Clark (1968), Prasad (1970), and Stockley (2002), and for galagos in particular from Anderson (2000), Perkin (2007), and Veerman (2010). I also used the Web site of the Nocturnal Primate Research Group at Oxford Brookes University, UK.