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  Notes

  The page numbers on these notes refer to the printed version of this book. The link provided will take you to the beginning of that print page. You may need to scroll forward from that location to find the corresponding note reference on your e-reader.

  Preliminaries

  1 Nowadays, the Netherlands Natural History Museum is housed in a modern building at the Bio Science Park of Leiden—and has been renamed Naturalis Biodiversity Center (www.naturalis.nl). The collection of antlers and the whale painting (depicting a beached sperm whale on the beach of Brouwershaven, 1606) are also there.

  1 The Sex Life of Wild Animals is Burns (1953).

  1 The classroom wall poster Penises of the Animal Kingdom was produced by Jim Knowlton (who received an Ig Nobel Prize for it in 1992).

  1 The online series Green Porno can be viewed via www.sundancechannel.com/greenporno.

  2 Darwin’s (1871) denial of primary sexual characteristics as being under sexual selection is outlined on pp. 253–54 of his Chapter 8 (“Principles of Sexual Selection”).

  2 Waage (1979) and Eberhard (1985) are listed in the bibliography.

  The conditions under which Waage began his damselfly genital studies are from an online interview I conducted with him on March 14, 2013.

  3 The events surrounding the conception of Eberhard’s book are from an e-mail correspondence with Bill Eberhard in late April 2013.

  4 The comment by Stephen Hubbell is from my book The Loom of Life (Schilthuizen, 2009).

  5 The female genitalia of the chimpanzee is described in Dahl (1985).

  5 The male genitalia of the chimpanzee is described in Prasad (1970).

  6 A paper in Nature (Barron and Brown, 2012) attacks the tendency for sensationalism and misreporting of sexual selection research by the science media.

  Chapter 1: Define Your Terms!

  9 Current views on bacterial sex are described in Prasad Narra and Ochman (2006).

  10 Mass spawning in coral is described in, for example, Harrison et al. (1984).

  10 Descriptions of sperm transfer without direct contact between males and females is described for pseudoscorpions, springtails (Collembola), and salamanders in Weygoldt (1969), Schaller (1971), and Houck and Verrell (2010), respectively.

  10 A good overview of the different sperm transfer methods among animals is Clark (1981).

  10 The theory that spermatophore deposition predated the evolution of genitalia is to be found in several chapters in Highnam (1964).

  10 More information on asexual reproduction in plants, parasitic wasps, stick insects, beetles, turkeys, lizards, and bdelloid rotifers can be found in Calzada et al. (1996), Godfray (1994), Bullini and Nascetti (1990), Dybas (1978), Olsen (1966), Radtkey et al. (1995), and Fontaneto et al. (2007), respectively.

  11 The various theories for the origin of sexual reproduction are explained in a very accessible way by Ridley (1993).

  13 Background on the evolution of the sexes is in Hoekstra (1987), Randerson and Hurst (2001), and Schilthuizen (2004). This and the previous section were checked by Rolf Hoekstra.

  14 A representative medical definition of primary vs. secondary sexual characteristics may be found in Haeberle (1983).

  15 Darwin (1871, Part II: 253–55) describes Hunter’s (1780) primary and secondary characteristics and problems in defining them in animals. A modern treatment of the same is in Ghiselin (2010).

  15 The genitalia of Cycloneda sanguinea are described in Eberhard (1985: 158) and Araújo-Siqueira and Almeida (2006).

  16 The blue testicles of male l’Hoest monkeys and mouse opossums are described in Prum and Torres (2004).

  16 More background on the discovery of sexual selection can be found in Chapter 4 of my book Frogs, Flies, and Dandelions (Schilthuizen, 2000).

  17 Ghiselin’s critique of the use of the term “character” is in, for example, Ghiselin (1984).

  18 Eberhard’s discussion of the definition of genitalia is in Eberhard (1985: 2).

  18 A good discussion on the evolution of internal fertilization as a result of life on land is Clark (1981).

  19 Van Leeuwenhoek (1678) was the first to describe (in Latin, because of the sensitive nature of the subject) the death of dog sperm cells in freshwater.

  19 A detailed figure showing the life span of various fish species’ sperm cells in distilled water of a range of temperatures is in Lindroth (1947).

  20 The medical cases of “infection” with squid sperm are described and interpreted zoologically by Marian et al. (2012) and also by Danna Staal in a videotaped performance on Nerd Night San Francisco (June 20, 2012). The headline quoted was from the June 15, 2012, online issue of the UK’s Daily Mail, based on a paper by Park et al. (2012).

  21 Tinbergen (1939) describes the mating behavior in Sepia cuttlefish.

  23 The information on hectocotylus autotomy in Argonauta is from Laptikhovsky and Salman (2003) and Sukhsangchan and Nabhitabhat (2007).

  23 The argonaut shell, which I briefly allude to, is a source of much speculation, since it is so similar to an ammonite shell and yet is made of a different material (calcite vs. aragonite) and not by the animal’s mantle, but by its tentacles. For this reason Naef (1921) has suggested that, when ammonites were not yet extinct, the ancestors of argonauts began using discarded ammonite shells for laying their eggs in, and over time evolved the ability to repair them and, eventually, to handcraft them themselves. This fanciful suggestion is not taken seriously by many, though. Another fascinating aspect of argonaut life is that they sometimes seem to live in symbiosis with jellyfish (the females) and salps (the males). A good video with basic information on argonauts is at museumvictoria.com.au/about/mv-news/2010/argonaut-buoyancy/.

  23 Cuvier’s description of Hectocotyle octopodis is in Cuvier (1829).

  24 Sedgwick’s paper read to the Royal Society is Sedgwick (1885).

  Group hunting in social onychophorans was described by Reinhard and Rowell (2005).

  25 The strange new head structures were first reported by Tait and Briscoe (1990). Tait and Norman (2001) described the mating behavior in Florelliceps stutchburyae. The discovery that onychophorans with head structures also maintain organs for fertilization through the skin is in Walker et al. (2006).

  Chapter 2: Darwin’s Peep Show

  The first seven hundred words of this chapter were published, in Dutch and in altered form, as Schilthuizen (2013).

  28 My visit to the Jardin des Plantes and the Muséum National d’Histoire Naturelle in Paris, in search of René Jeannel’s statue, took place on July 16, 2012.

  29 Information on Jeannel’s biography I took from Motas (1966), Negrea (2007), and d’Aguilar (2007), and from the page on René Jeannel at fr.wikipedia.org/wiki/René_Jeannel.

  29 The information on cave art discovered by Jeannel is mentioned in Lawson (2012).

  29 Jeannel’s doctoral thesis is Jeannel (1911). Leptodirini, a tribe in the small fungus beetle family Leiodidae, were in Jeannel’s days called Bathysciinae and considered to be a subfamily of the carrion beetles, Silphidae.

  31 Jeannel’s monograph of the “aedeagus” is Jeannel (1955).

  31 Examples of bumblebee taxonomy are Williams (1991) and Richards (1927), although the species specificity of the bumblebee penis was already noted by V. Audoin in 1821 (Jeannel, 1955).

  31 More information on bumblebee genitalia can be found at www.nhm.ac.uk/research-curation/research/projects/bombus/genitalia.html.

  31 More information on bumblebees in general can be found at www.bumblebee.org and bumblebe
econservation.org. Although bumblebees predominate in the Northern Hemisphere, some species occur in South America and the mountainous parts of Southeast Asia.

  32 Some background on elephant shrews and their classification can be found in Springer et al. (1997) and Dawkins (2004: 224); the study on male genital shapes in these animals is Woodall (1995), whereas some background on the female reproductive system is in Tripp (1971).

  34 In Chapter 4 of my book Frogs, Flies, and Dandelions (Schilthuizen, 2000), I place genital diversity in the context of speciation (see also Afterplay in the present book).

  34 The entomologist who impressed me at a Netherlands Entomological Society meeting (in the winter of 1981–1982) was Mr. Diakonoff.

  34 The paragraphs on Maria Cardoso were based on a documentary by the Australian Broadcasting Corporation, online at www.abc.net.au/arts/artists/maria-fernanda-cardoso-the-museum-of-copulatory- organs/default.htm, the artist’s own Web site, www.mariafernandacardoso.com, and e-mail exchanges with her throughout the writing of this book.

  36 Gosse’s quote is from Gosse (1883). I must admit that I, as many people before me, have quoted Gosse deliberately out of context. Gosse actually goes on to state that although the view of genitalia as locks and keys is often expressed, “I should like to see these axioms demonstrated.”

  36 Further background on the lock-and-key hypothesis can be found in, for example, Eberhard (1985) and Shapiro and Porter (1989).

  36 In this section, I combine the “mechanical” and the “sensory” versions of the lock-and-key hypothesis. The latter is worded in, for example, Jeannel (1941, 1955) and De Wilde (1964).

  36 The paper on carrion beetles in a Czech forest is by Kočárek (2002), and illustrations of the penises of Catops species may be found in, for example, Jeannel (1936).

  37 Fooden (1967) described the macaque genitalia.

  37 Lock-and-key theories were questioned for bumblebees by, for example, Richards (1927) and Boulangé (1924).

  37 The entomologist who showed me his cross-species copulas was the late Jan Lucas.

  39 The mating experiments on chiral Ciulfina are described in Holwell and Herberstein (2010).

  39 The biogeographic evidence against the lock-and-key hypothesis is in Eberhard (1985), but also Shapiro and Porter (1989), Eberhard (1996), Arnqvist (1997), and Eberhard and Huber (2010).

  40 The example of lock-and-key-like patterns in Drosophila is from Kamimura and Mitsumoto (2012).

  Chapter 3: An Internal Courtship Device

  42 The field guides mentioned are Jeyarajasingam and Pearson (1999), Kleukers et al. (1997), and Freude et al. (1971).

  44 Eberhard’s quote is from Eberhard (1985: 15).

  44 The Darwin caricature is by Albert Way (1805–1874) and is held by the Cambridge University Library. (As far as we know Darwin never rode any giant beetle—only giant tortoises.) The account of his beetle-collecting days is from Barlow (1958: 62–63).

  44 Darwin’s barnacle treatises are Darwin (1851, 1854).

  44 In Darwin’s 1854 monograph, he describes the penis of the burrowing barnacle (according to Birkhead, 2009) as “wonderfully developed . . . when fully extended, it must equal between eight and nine times the entire length of the animal . . . coiled up, like a great worm.”

  44 The list of longest penises in the animal kingdom is in Neufeld and Palmer (2008).

  44 More details on barnacle penis morphology are in Hoch (2008) and Neufeld and Palmer (2008), while a video of mating barnacles can be found at vimeo.com/7461478.

  45 The influence of Henrietta Darwin on her father’s work is described in, for example, Birkhead (2007, 2008, 2009), while the anecdote on her stinkhorn campaign comes from Raverat (1952) (fide Birkhead, 2007). I also used notes made during Birkhead’s Tinbergen Lecture at Leiden University on May 11, 2012. Her diary, as well as a commentary on it, is published at www.darwinproject.ac.uk/hed-diary-1871. Henrietta’s denial of the “Lady Hope Story” of Darwin’s deathbed change of heart is in Litchfield (1922).

  47 Bateman (1948) became a key paper in the development of sexual selection theory after it was “rediscovered” by Trivers (1972). However, Bateman (1948) made errors in his experimental design and in the analysis of his results, which were highlighted by Gowaty et al. (2012), who also repeated his experiments and found no evidence for sexual selection. Other criticisms of Bateman’s principle have been summarized by Judson (2002). The section on Bateman’s principle was read and commented upon by Hanna Kokko, who shared with me two unpublished (partial) book chapters by her on the subject, and also pointed me to the paper by Gerlach et al. (2012), which explains why positive Bateman gradients for females might be statistical artifacts.

  48 A popular account of the history of sexual selection, especially the “female choice” version of it, is in Schilthuizen (2000). In that book, I adhere to the conceptual difference between “good genes” and “Fisherian” sexual selection—see also Ridley (1993). However, as, for example, Kokko et al. (2003) have shown, there is no basic difference between the two.

  50 The work on sexual selection in poison frogs is in Maan and Cummings (2008, 2009, 2012). For more information on this system, see Myers and Daly (1976) and Summers (2004).

  51 The examples of female choice in peacocks and barn swallows are from Petrie (1994) and Møller (1990), respectively.

  51 The original discovery of the effect of leg bands on female choice is in Burley et al. (1982).

  51 Burley’s work on the effect of head crests is in Burley and Symanski (1998), whereas the information on a change in behavior of males made artificially attractive is in Burley (1988).

  52 Sensory drive is a complex process with several components that have been separately studied and named. Endler and Basolo (1998) paint a coherent picture of all this.

  53 Visual penis display in mosquito fish, primates, and lizards is described in, respectively, Kahn et al. (2010), Wickler (1966), and Bohme (1983), whereas Mautz et al. (2013) is the reference for the study on human penis length as a factor in male visual attractiveness. The squirrel monkey example comes from Ploog and MacLean (1963).

  54 The cartoons of Rube Goldberg can be found at rubegoldberg.com.

  54 The paper on stridulating genitals in crane flies is Eberhard and Gelhaus (2009), whereas papers on genital stridulation in moths are, for example, Heller and Krahe (1994) and Conner (1999).

  55 The function of parameres in general is described in Eberhard (1985) and more specifically in beetles in Düngelhoef and Schmitt (2010). Please note: the sentence placed in quotation marks (“more to the left—yes, that’s it”) is not intended to be quoting Dr. Düngelhoef. Parameres in the ladybird beetle Cycloneda are described in, for example, Araújo-Siqueira and Almeida (2006) and a video of a mating pair (with paramere action!) is at www.youtube.com/watch?v=VplJpd lUmsw.

  57 The penile flagella in insects are described in Eberhard (1985) and Rodriguez et al. (2004), while the urethral processes in hoofed mammals are in Prasad (1970). The report that in cow copulation this process flips forward is from Eberhard (1985: 11).

  57 The cultural anthropology of the Bornean palang is described with relish in Harrisson (1959); the Sarawak Museum in Malaysia holds several famed examples.

  57 The quotation on wasp genitalia is from West-Eberhard (1984).

  57 The proportions of species in which rhythmic genital thrusting occurs, including the detail on the bush baby, as well as the observations on “cryptic thrusting,” are taken from Eberhard (1996).

  58 The phalloid organ of the red-billed buffalo weaver and its use in copulation is described in Winterbottom et al. (1999, 2001) and in the Tinbergen Lecture by Tim Birkhead at Leiden University on May 11, 2012.

  58 The sense organs in the damselfly vagina, cockroach female genitals, human clitoris, and human vagina are derived from Córdoba-Aguilar (2005), Eberhard (2010a), Cold and McGra
th (1999), and Pauls et al. (2006), respectively.

  58 An example of the heritability of genital shape is Sasabe et al. (2007).

  59 The two back-to-back papers in Animal Behaviour are Baker and Bellis (1993a, b), and the details in this section are from these two papers, as well as from a conversation I had with Robin Baker during the Sixth Congress of the European Society for Evolutionary Biology, Arnhem, August 24–28, 1997.

  59 Baker’s later work has been criticized by, among others, Tim Birkhead, first mildly (Birkhead, 1995), later more vehemently (Birkhead et al., 1997).

  61 The quotation on Baker and Bellis’s popularity during the Princeton congress is from Birkhead (1995).

  61 The female genitalia of the spider Silhouettella loricatula and how they might function in the species’ habit of sperm dumping are described in Burger et al. (2006) and Burger (2007).

  62 Sperm dumping in cellar spiders is described in Peretti and Eberhard (2009), in Grevy’s zebra in Ginsberg and Huck (1989) and Ginsberg and Rubenstein (1990), and in chickens in Dean et al. (2011). The description of the copulation and sperm dumping in the nematode worm Caenorhabditis elegans is in Barker (1994). The thrusting movements of nematode spicules during copulation, as well as further details about mating, are described in Barr and Garcia (2006).

  Chapter 4: Fifty Ways to Peeve Your Lover

  65 The quotes from Eberhard’s book are all from Eberhard (1996).

  66 Some of Donald Dewsbury’s papers that I consulted are Dewsbury (1971, 1974) and Langtimm and Dewsbury (1991).

  67 Another early author to describe a “dry” phase in spider copulation was Kullmann (1964).

  67 Dry sex in millipedes is described in, for example, Tanabe and Sota (2008). The examples of other animals are taken from Eberhard (1985).

  67 I interviewed Peter van Helsdingen in Leiden on October 25, 2012. His paper is Van Helsdingen (1965).