External genital morphology of the ring-tailed lemur (Lemur catta): females are naturally "masculinized".
The extravagance and diversity of external genitalia have been well characterized in male primates; however, much less is known about sex differences or variation in female form. Our study represents a departure from traditional investigations of primate reproductive anatomy because we 1) focus on external rather than internal genitalia, 2) measure both male and female structures, and 3) examine a strepsirrhine rather than an anthropoid primate. The subjects for morphological study were 21 reproductively intact, adult ring-tailed lemurs (Lemur catta), including 10 females and 11 males, two of which (one per sex) subsequently died of natural causes and also served as specimens for gross anatomical dissection. Male external genitalia presented a typical masculine configuration, with a complex distal penile morphology. In contrast, females were unusual among mammals, presenting an enlarged, pendulous external clitoris, tunneled by the urethra. Females had a shorter anogenital distance and a larger urethral meatus than did males, but organ diameter and circumference showed no sex differences. Dissection confirmed these characterizations. Noteworthy in the male were the presence of a "levator penis" muscle and discontinuity in the corpus spongiosum along the penile shaft; noteworthy in the female were an elongated clitoral shaft and glans clitoridis. The female urethra, while incorporated within the clitoral body, was not surrounded by erectile tissue, as we detected no corpus spongiosum. The os clitoridis was 43% the length and 24% the height of the os penis. On the basis of these first detailed descriptions of strepsirrhine external genitalia (for either sex), we characterize those of the female ring-tailed lemur as moderately "masculinized." Our results highlight certain morphological similarities and differences between ring-tailed lemurs and the most male-like of female mammals, the spotted hyena (Crocuta crocuta), and call attention to a potential hormonal mechanism of "masculinization" in female lemur development.
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