The developing renal, reproductive, and respiratory systems of the African elephant suggest an aquatic ancestry

Abstract

The early embryology of the elephant has never been studied before. We have obtained a rare series of African elephant (Loxodonta africana) embryos and fetuses ranging in weight from 0.04 to 18.5 g, estimated gestational ages 58-166 days (duration of gestation is approximately 660 days). Nephrostomes, a feature of aquatic vertebrates, were found in the mesonephric kidneys at all stages of development whereas they have never been recorded in the mesonephric kidneys of other viviparous mammals. The trunk was well developed even in the earliest fetus. The testes were intra-abdominal, and there was no evidence of a gubernaculum, pampiniform plexus, processus vaginalis, or a scrotum, confirming that the elephant, like the dugong, is one of the few primary testicond mammals. The palaeontological evidence suggests that the elephant's ancestors were aquatic, and recent immunological and molecular evidence shows an extremely close affinity between present-day elephants and the aquatic Sirenia (dugong and manatees). The evidence from our embryological study of the elephant also suggests that it evolved from an aquatic mammal.

Figure 1

The youngest and oldest African elephant embryo and fetus used for this study. (A) Embryo, estimated gestation 58 days. (B) Fetus, estimated gestation 166 days. [Bars = 5 mm.]

Figure 2

Growth of the African elephant fetus. Fetal weight (A), crown-rump length (B), and trunk length (C) increase with estimated gestational age.

Figure 3

Histological appearance of the mesonephric kidneys and lungs of African elephant fetuses. (A) Transverse section through the 115-day fetus showing the mesonephros with nephrostomes (N) opening into the coelom (Co) and connecting to the glomerulus (G) and associated collecting tubules (T). (B) High-power photomicrograph of one mesonephric nephrostome (N) clearly showing cilia (Ci). The cilia are characteristically angled inwards indicating the direction of flow of the filtrate. (C) Transverse section through the 139-day fetus showing mesonephros (M), metanephros (Me), dorsal aorta (da), and the posterior vena cava (pvc). The future spermatic vein (sv) leads directly from the mesonephros and the developing testis (not shown) to the posterior vena cava. (D) Transverse thoracic section through the 139-day fetus showing lung (L) and pleural cavity (Pl), heart (H) surrounded by pericardium, dorsal aorta (da), oesophagus (oe), and bronchus (B). [Bars = 0.25 mm (A), 0.16 mm (B), 0.64 mm (C), and 0.75 mm (D).]

Figure 4

The number of nephrostomes, renal tubules, and glomeruli in the mesonephric kidney of the African elephant. Shown are Nephrostomes (●), tubules (▵), and glomeruli (▿).

Figure 5

Diagram and photograph of the ventral view of a dissected 166-day African elephant fetus. (A) This shows the short, straight spermatic vein (sv) and spermatic artery (sa). The right testis (RT) and Wolffian duct are displaced caudally (indicated by dotted outline) to show the course of the renal vein (rv) and the renal artery (ra) supplying the metanephric kidney (K) and the ureter (U). The right mesonephros has been omitted for clarity. The gut (G) has been removed, and the bladder (B) has been reflected caudally. Note that the adrenal glands (Ad) are large. The metanephric kidney is lobular as in the adult. The mesonephros (M) is regressing. (B) The large intra-abdominal testes (T) on the ventral aspect of the lobular metanephric kidney (K) are evident. The regressing mesonephros (M) is just visible. The gut (G) has been removed, and the bladder (B) has been reflected caudally.