Reduced heterozygosity impairs sperm quality in endangered mammals

Abstract

Inbreeding causes increases in homozygosity and is commonly associated with reductions in fertility and embryogenesis. Although the mechanisms underlying such effects are unknown, recent work has suggested that inbred males may suffer impaired ejaculate quality, thus providing a functional explanation for reductions in reproductive function in inbred populations. However, the relationship between inbreeding and sperm quality remains controversial, particularly in wild populations where the level of inbreeding is typically estimated using neutral molecular markers. Such markers are thought to reflect genome-wide levels of heterozygosity only under restricted conditions, and rarely in outbred populations. Here we employ a comparative approach that takes account of these criticisms and evaluates the evidence linking inbreeding to reductions in sperm quality in 20 mammal species. We focus on sperm abnormalities and sperm motility, which are key determinants of male fertility in many species. We show that species with reduced mean heterozygosity have impaired ejaculated quality, although subsequent analyses revealed that these effects were confined to endangered populations. Our findings therefore support the notion that inbreeding can severely impair sperm quality while concomitantly addressing criticisms surrounding the use of heterozygosity estimates to estimate the level of inbreeding.

Figure 1

Relationship between the proportion of (a) abnormal and (b) motile sperm in endangered (filled circles, solid line) and non-endangered (open circles, broken line) mammals. Data in the figures are not controlled for phylogeny. Numbers indicate the species: (1) Florida panther, (2) Indian lion, (3) cheetah, (4) black-footed ferret, (5) Ngorongoro Crater lion, (6) black bear, (7) South American panther, (8) margays, (9) tigrinas, (10) red wolf, (11) jaguar, (12) giant panda, (13) ocelot, (14) brown bear, (15) European rabbit, (16) Serengeti lions, (17) howler monkey, (18) bison, (19) domestic cat, (20) coyotes. See electronic supplementary material for additional details.