He makes two main points here that I think are worth engaging with further. The second one (communal caregiving among foragers), I will save for a later date, to focus narrowly here on the first.

The first point is in regard to the suite of features that Ryan argues testify “in support of ancestral promiscuity.” These being: “penis morphology, repeated thrusting movement, frequent non-reproductive sexual behavior, female multiple orgasm, female copulatory vocalization, etc.).”

Let’s consider penis morphology. I will quote at length the case Ryan makes regarding the uniqueness of the human penis in Sex at Dawn:

Despite its lack of curlicues, the human penis is not without interesting design features. Primate sexuality expert Alan Dixson writes, “In primates which live in family groups consisting of an adult pair plus offspring [such as gibbons] the male usually has a small and relatively unspecialized penis.” Say what you will about the human penis, but it ain’t small or unspecialized. Reproductive biologist Roger Short (real name) writes, “The great size of the erect human penis, in marked contrast to that of the Great Apes, makes one wonder what particular evolutionary forces have been at work.” Geoffrey Miller just comes out and says it: “Adult male humans have the longest, thickest, and most flexible penises of any living primate.” So there.

Homo sapiens: the great ape with the great penis!

The unusual flared glans of the human penis forming the coronal ridge, combined with the repeated thrusting action characteristic of human intercourse—ranging anywhere from ten to five hundred thrusts per romantic interlude—creates a vacuum in the female’s reproductive tract. This vacuum pulls any previously deposited semen away from the ovum, thus aiding the sperm about to be sent into action. But wouldn’t this vacuum action also draw away a man’s own sperm? No, because upon ejaculation, the head of the penis shrinks in size before any loss of tumescence (stiffness) in the shaft, thus neutralizing the suction that might have pulled his own boys back. Very clever.

Intrepid researchers have demonstrated this process, known as semen displacement, using artificial semen made of cornstarch (the same recipe used to simulate exaggerated ejaculates in many pornographic films), latex vaginas, and artificial penises in a proper university laboratory setting. Professor Gordon G. Gallup and his team reported that more than 90 percent of the cornstarch mixture was displaced with just a single thrust of their lab penis. “We theorize that as a consequence of competition for paternity, human males evolved uniquely configured penises that function to displace semen from the vagina left by other males,” Gallup told BBC News Online. (Ryan, 234).

Broadly, we can break Ryan's argument down into a number of specific claims:

1) The human penis has “interesting [unique] design features,” it’s “specialized.”

2) The human penis is, among other virtues, the “longest…of any living primate.” (according to Geoffrey Miller, and quoted favorably by Ryan)

3) The flared glans of the human penis is “unusual” and that, according to Gordon G. Gallup, “as a consequence of competition for paternity, human males evolved uniquely configured penises that function to displace semen from the vagina left by other males.”

Now, Sex at Dawn was published in early 2010; however, in 2009, a book was published by primatologist Alan Dixson, who Ryan accurately describes as a “primate sexuality expert.” Ryan repeatedly quotes Dixson’s work from the late 1990’s and early 2000’s in Sex at Dawn, but I’m guessing Dixson’s 2009 book, Sexual Selection and the Origins of Human Mating Systems, was published too late for Ryan to integrate his insights from that work into his own, since it is not referenced.

This is unfortunate, because Dixson offers a pretty comprehensive breakdown for why each of these claims are likely mistaken.

First, the human penis actually seems to be comparatively quite dull in terms of “design features”. Here are illustrations from Dixson’s work on the penile morphology of various primates.