Osteological evidence for the evolution of activity pattern and visual acuity in primates.
Examination of orbit size and optic foramen size in living primates reveals two adaptive phenomena. First, as noted by many authors, orbit size is strongly correlated with activity pattern. Comparisons of large samples of extant primates consistently reveal that nocturnal species exhibit proportionately larger orbits than diurnal species. Furthermore, nocturnal haplorhines (Tarsius and Aotus) have considerably larger orbits than similar-sized nocturnal strepsirrhines. Orbital hypertrophy in Tarsius and Aotus accommodates the enormously enlarged eyes of these taxa. This extreme ocular hypertrophy seen in extant nocturnal haplorhines is an adaptation for both enhanced visual acuity and sensitivity in conditions of low light intensity. Second, the relative size of the optic foramen is highly correlated with the degree of retinal summation and inferred visual acuity. Diurnal haplorhines exhibit proportionately larger optic foramina, less central retinal summation, and much higher visual acuity than do all other primates. Diurnal strepsirrhines exhibit a more subtle but significant parallel enlargement of the optic foramen and a decrease in retinal summation relative to the condition seen in nocturnal primates. These twin osteological variables of orbit size and optic foramen size may be used to draw inferences regarding the activity pattern, retinal anatomy, and visual acuity of fossil primates. Our measurements demonstrate that the omomyiforms Microchoerus, Necrolemur, Shoshonius, and Tetonius, adapiform Pronycticebus, and the possible lorisiform Plesiopithecus were likely nocturnal on the basis of orbit diameter. The adapiforms Leptadapis, Adapis, and Notharctus, the phylogenetically enigmatic Rooneyia, the early anthropoids Proteopithecus, Catopithecus, and Aegyptopithecus, and early platyrrhine Dolichocebus were likely diurnal. The activity pattern of the platyrrhine Tremacebus is obscure. Plesiopithecus, Pronycticebus, Microchoerus, and Necrolemur probably had eyes that were very similar to those of extant nocturnal primates, with a high degree of retinal summation and rod-dominated retinae. Leptadapis and Rooneyia likely had eyes similar to those of extant diurnal strepsirrhines, with moderate degrees of retinal summation, a larger cone:rod ratio than in nocturnal primates, and, more speculatively, well-developed areae centrales similar to those of diurnal strepsirrhines. Adapis exhibited uncharacteristically high degrees of retinal summation for a small-eyed (likely diurnal) primate. None of the adapiform or omomyiform taxa for which we were able to obtain optic foramen dimensions exhibited the extremely high visual acuity characteristic of extant diurnal haplorhines.
Kay
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RF
Department of Biological Anthropology and Anatomy, Duke University Medical Center, Durham, North Carolina 27710, USA. Rich_Kay@baa.mc.duke.edu
Kirk
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EC
D000818:Animals; D005075:Biological Evolution; D005123:Eye / Q000033:anatomy & histology; D009915:Orbit / Q000033:anatomy & histology; D011323:Primates / Q000033:anatomy & histology / Q000502:physiology*; D012160:Retina / Q000502:physiology; D014792:Visual Acuity