Evolution favors protection of developing germ cells, the precursors for the next generation, from environmental insults that may increase the number of deleterious mutations in the genome, or that may otherwise interfere with normal development of sperm or eggs. Elevated temperature is one such insult that is known to increase the mutation rate and to cause abnormal spermatid differentiation (spermiogenesis) in mammals. Descent of the testes, and development of a scrotum outside the abdominal wall, are two mechanisms, hypothesized to have been selected for during mammalian evolution, which reduce temperature-related damage to developing sperm. Because male turtles, crocodiles, birds, and monotremes (platypus, echidna) have undescended, intra-abdominal testes (a condition known as testicond), it has long been assumed that testicondy is the primitive condition for all mammalian lineages. However, recent mapping of three "character states" for testicular position and existence of a scrotum (see Figure 1 below; Werdelin and Nilsonne, 1999) onto the revised phylogeny of Mammalia indicates that descended, scrotal testicles may instead be the primitive condition for a clade that includes most eutherians (placental mammals).
Figure 1. Three "character states" for the testes of male mammals: a) testicond (not descended) in the Rufous Elephant Shrew, b) descended but no scrotum in the Harbor Seal, c) descended and scrotal, in the horse. From Werdelin and Nilsonne, 1999
Elephants comprise one group of truly testicond mammals; with a core body temperature above 36C, and no identified cooling mechanism for the intra-abdominal testicles, these proboscideans appear to violate the temperature hypothesis for evolution of the scrotum and testicular descent (Werdelin and Nilsonne, 1999). Other mammals that are truly testicond, such as tenrecs, golden moles, and monotremes, have relatively low core body temperatures. The exceptional elephants have close relatives that regulate testicular temperature in two different manners. Hyraxes (Hyracoidea) have poor internal thermoregulation, and thus control core temperature behaviorally; also, reproduction is seasonal in these animals, such that continuous production of sperm is not required.
The Sirenia (dugongs and manatees) are also close relatives of elephants, and the reproductive organs of the Florida Manatee (Trichechus manatus latirostris) would seem to be at risk, due to insulating fat, proximity to heat-generating swimming muscles, and a core body temperature of 36C. Therefore, Rommel and colleages (2001) examined the vascular anatomy of structures surrounding the reproductive organs in both male and female manatees, obtained as carcasses necropsied by the Florida Fish and Wildlife Conservation Commission. After removing ventral skin, fat and abdominal muscle to expose the organs, the researchers focused their attention on the anatomy of a region called the hypogastric fossa, where body wall thickness is reduced. Veins and arteries in this region were injected with colored latex, through the caudal vena cava, and the aorta, respectively.
Figure 2. Ventral view of the positions of the reproductive organs in the hypogastric fossae of male and female manatees. From Rommel et al., 2001
In the manatee, the intra-abdominal testes are located just caudal and lateral to the kidneys, and the epididymides, where sperm are stored and undergo maturation, extend towards the tail of the animal, into the hypogastric fossae. The body wall is three to four times thinner in this area, and lined by two flat plexuses of blood vessels. One plexus is the arteriovenous iliac vascular bundle, consisting of triads with one artery plus a pair of veins. The other plexus is consists of connections (anastomoses) between large-diameter veins, and is called the inguinal venous plexus. Rommel and colleagues identified fan-shaped vascular arrays, the superficial thoracocaudal plexuses, which feed cooled blood into the inguinal venous plexus, at the margin of the hypogastric fossa. They propose that this anatomical arrangement allows cooling of the epididymides by heat transfer to the inguinal venous plexus, which is receiving cooled blood from the periphery via the superficial thoracocaudal plexuses.
Figure 3. Comparison of thermoregulation mechanisms in manatees, dolphins, and seals. From Rommel et al., 2001
Figure 3 above shows a comparison of vascular adaptations in manatees, dolphins, and seals. In the dolphin, cooled venous blood entering the lumbocaudal venous plexus undergoes countercurrent heat exchange with arterial blood supplying the testis and epididymis, from the spermatic arterial plexus. Veins from the dorsal fin and flukes contribute to this exchange. In phocid seals, cooled venous blood drains from the surfaces of the hind flippers, and cools the testes and epididymides directly, through an inguinal venous plexus. The testes have descended from the embryonic position in seals, but there is no scrotum, and these reproductive organs remain para-abdominal. Although the focus in this paper is on thermoregulation of the male reproductive organs, the presence of similar vascular structures in females leads the authors to speculate that they may function to prevent increases in fetal temperature.
References:
Werdelin, L. and Nilsonne, A (1999) The evolution of a scrotum and testicular descent in mammals: a phylogenetic view. J. Theoret. Biol. 196, 61-72.
Rommel, S., Pabst, D., & McLellan, W. (2001). Functional morphology of venous structures associated with the male and female reproductive systems in Florida manatees (Trichechus manatus latirostris) The Anatomical Record, 264 (4), 339-347 DOI: 10.1002/ar.10022
