Mother and infant owl monkeys (painting by Anne-Elise Martin photographed by Lu Yao).
Successful fertilization generally requires very large numbers of sperm. Men, for example, are increasingly likely to become infertile if sperm counts decline below 70 million per ejaculate, about a quarter of the average of about 250 million. Comparable figures apply for various domesticated mammals. So it is surprising that New World owl monkeys have exceedingly low sperm counts.
Alarming report from a primate centre
Reviewing abnormal sperms in human ejaculates for my previous post (October 16: Kamikaze Sperms or Flawed Products?) reactivated a long-suppressed memory of a nail-biting encounter with low sperm counts in owl monkeys. Forty years ago, I was appointed to lead the Wellcome Laboratories of Comparative Physiology at the Zoological Society of London. Discussions with Alister Voller revealed that owl monkeys were the only non-human primates successfully infected with human malaria. They seemed likely to become a laboratory model for developing new approaches to malaria treatment, so I decided to launch a study of their reproductive biology to promote breeding in captivity.
With grants from the World Health Organization and the Wellcome Trust, I founded a colony of owl monkeys and engaged Alan Dixson as the postdoc. (Thus began our long-lasting scientific collaboration and friendship.) After setting things up, all we had to do was to wait for breeding to occur. But then a frightening publication from the New England Primate Research Center hit our desks. To investigate breeding failure in a large colony of owl monkeys, Ronald Hunt and colleagues took 200 testicular biopsies from males. None showed a normal pattern of sperm production. In most cases, tubules in the testes contained no sperms at all. Hunt and colleagues excluded seasonal variation as an explanation. Making bad news considerably worse, they inferred that vitamin E deficiency had irreversibly arrested sperm production in their colony.
Alan immediately conducted biopsies on 15 of our males, with similarly depressingly results. A colleague commented that images from the biopsies resembled those from testes of the mule (an infertile hybrid). Later on, sectioned testes from four adult males did reveal the presence of a few sperms in some seminiferous tubules. In contrast to other primates, electroejaculation was largely unsuccessful, but did yield small emissions containing a few sperms.
Breeding with almost no sperms
After several anxious months, Alan and I were enormously relieved when our caged pairs of owl monkeys eventually began to produce offspring. We feared the worst because copulation occurred very infrequently in established pairs, but regular breeding nevertheless ensued. Five males in breeding pairs showed the usual picture of limited sperm production, and one male successfully fertilized a female within a few days of testicular biopsy.
The inference that minimal sperm production seen in owl monkeys is due to vitamin E deficiency does not stand up. Males that grew up in our breeding colony, with a diet including normal vitamin E levels, had the same testicular pattern when adult. Moreover, the pattern was not altered by giving one growing male an extra daily dose of vitamin E. Testes of wild-living owl monkeys have yet to be examined, but available evidence indicates that very limited sperm production is universal. As Alan Dixson noted in 1994: “How these monkeys, which copulate infrequently and produce so few spermatozoa, are able to impregnate their female partners remains a mystery.”
Implications for sperm competition
Owl monkeys are known to have relatively small testes and little sexual dimorphism in body size or appearance. These features fit their typical pair-living habits. Field studies conducted first by Patricia Wright and subsequently by Eduardo Fernandez-Duque have established that social monogamy is the norm. Owl monkeys are also best kept in pairs in captivity. Both wild and captive pair-living males participate in infant carriage, another feature generally associated with monogamy. Everything points to the inference that sperm competition should be virtually absent in owl monkeys. So they would be expected to produce fewer sperms than primates living in multi-male groups. However, no other monogamous primate shows the extreme reduction in sperm production found in owl monkeys. Moreover, recent findings indicate that there may be some degree of intra-sexual competition. Long-term data from groups studied by Fernandez-Duque and his team have revealed that solitary “floaters” of both sexes may incur intense competition and aggression. On average, one of the original pair-mates is replaced every three years. So sperm competition might occasionally occur.
Owl monkeys also provide information on abnormal sperms in ejaculates. In 2006, Michelle Schuler and colleagues reported findings from a colony at the University of South Alabama. Because electroejaculation was unsuccessful, they used vibrostimulation to collect semen. They did manage to collect tiny ejaculates containing sperms from some males. However, over 80% of sperms were immotile and multiple abnormalities were seen, including overlarge or twinned heads, bent, broken or missing tails and aberrant midpieces. So minimal sperm production in owl monkeys is compounded by a high frequency of abnormalities. This provides further evidence that different kinds of sperms in primate ejaculates do not indicate adaptation for sperm competition but reflect poor quality control. And the extremely low sperm counts of owl monkeys have become even more mysterious.
Dixson, A.F. (1982) The owl monkey (Aotus trivirgatus). pp. 71-113 in: Reproduction in New World Primates (ed. Hearn, J.P.). Lancaster: MTP Press.
Dixson, A.F. (1994) Reproductive biology of the owl monkey. pp. 113-132 in: Aotus: The Owl Monkey (eds. Baer, J.F., Weller, R.E. & Kakoma, I.). San Diego: Academic Press.
Dixson, A.F. (2012) Primate Sexuality: Comparative Studies of the Prosimians, Monkeys, Apes and Human Beings (Second Edition). Oxford: Oxford University Press.
Fernandez-Duque, E. (2011) Aotinae: Social monogamy in the only nocturnal anthropoid. pp. 139-154 in: Primates in Perspective (Second Edition) (eds. Campbell, C.J., Fuentes, A., MacKinnon, K.C., Bearder, S.K. & Stumpf, R.). Oxford: Oxford University Press.
Fernandez-Duque, E. & Huck, M. (2013) Till death (or an intruder) do us part: Intrasexual-competition in a monogamous primate. PLoS One 8(1): e53724:1-5.
Hunt, R.D., Blake, B.J. & Chalifoux, L.V. (1993) Arrested spermatogenesis: Aotus trivirgatus, Saimiri sciureus, and Macaca mulatta. pp. 164-168 in: Nonhuman Primates (Monographs on Pathology of Laboratory Animals) (eds. Jones, T.C., Mohr, U. & Hunt, R.D.). Washington: International Life Sciences Institute.
Hunt, R.D., Chalifoux, L.V., King, N.W. & Trum, B.F. (1975) Arrested spermatogenesis in owl monkeys (Aotus trivirgatus). J. Med. Primatol., 4:399-400.
Schuler, A.M., Gibson, S.V. & Westberry, J.M. (2006) Sperm collection from owl monkeys (Aotus sp.). Am. J. Primatol., 68, Suppl.1:104-105. (Abstract only)
Wright, P.C. (1981) The night monkeys, genus Aotus. pp. 211-240 in: Ecology and Behavior of Neotropical Primates (eds. Coimbra-Filho, A.F. & Mittermeier, R.A.). Rio de Janeiro: Academia Brasileira de Ciências.