Eye Size at Birth in Prosimian Primates: Life History Correlates and Growth Patterns

Abstract Background: Primates have large eyes relative to head size, which profoundly influence the ontogenetic emergence of facial form. However, growth of the primate eye is only understood in a narrow taxonomic perspective, with information biased toward anthropoids

Eye Size at Birth in Prosimian Primates: Life History Correlates and Growth Patterns

BACKGROUND: Primates have large eyes relative to head size, which profoundly influence the ontogenetic emergence of facial form. However, growth of the primate eye is only understood in a narrow taxonomic perspective, with information biased toward anthropoids.\ud \ud METHODOLOGY/PRINCIPAL FINDINGS: We measured eye and bony orbit size in perinatal prosimian primates (17 strepsirrhine taxa and Tarsius syrichta) to infer the extent of prenatal as compared to postnatal eye growth. In addition, multiple linear regression was used to detect relationships of relative eye and orbit diameter to life history variables. ANOVA was used to determine if eye size differed according to activity pattern. In most of the species, eye diameter at birth measures more than half of that for adults. Two exceptions include Nycticebus and Tarsius, in which more than half of eye diameter growth occurs postnatally. Ratios of neonate/adult eye and orbit diameters indicate prenatal growth of the eye is actually more rapid than that of the orbit. For example, mean neonatal transverse eye diameter is 57.5% of the adult value (excluding Nycticebus and Tarsius), compared to 50.8% for orbital diameter. If Nycticebus is excluded, relative gestation age has a significant positive correlation with relative eye diameter in strepsirrhines, explaining 59% of the variance in relative transverse eye diameter. No significant differences were found among species with different activity patterns.\ud \ud CONCLUSIONS/SIGNIFICANCE: The primate developmental strategy of relatively long gestations is probably tied to an extended period of neural development, and this principle appears to apply to eye growth as well. Our findings indicate that growth rates of the eye and bony orbit are disassociated, with eyes growing faster prenatally, and the growth rate of the bony orbit exceeding that of the eyes after birth. Some well-documented patterns of orbital morphology in adult primates, such as the enlarged orbits of nocturnal species, mainly emerge during postnatal development.\ud \u

Eye diameter and activity pattern in newborn strepsirrhine primates.

<p>Left column, log10 transformed axial eye diameter, transverse eye diameter, and orbital aperture diameter plotted against cranial length in primates with different activity patterns. Note that all cathemeral and diurnal scale below the regression line for nocturnal primates. Right column: relative size (residuals) of the same measurements. Although no significant differences were found, nocturnal species show a trend toward relatively larger eye dimensions than cathemeral and diurnal species. The difference in orbital aperture dimensions is less apparent.</p

Relative transverse eye diameter (residuals calculated from regression of Log10 transverse eye diameter against Log10 cranial length) plotted against relative age at weaning (top) and relative gestational age (bottom).

<p>No relationship to relative neonatal body mass as apparent in our analysis (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0036097#pone-0036097-t005" target="_blank">Table 5</a>).</p

Cranial length and life history variables of the specimens used in statistical analyses.

<p>C, cathemeral; D, diurnal; N, nocturnal; CL, average cranial length (prosthion-inion) measured from this sample.</p>1<p>activity pattern according to Kirk, 2006 <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0036097#pone.0036097-Kirk1" target="_blank">[2]</a>.</p>2<p>neonatal mass, gestation length, and weaning age obtained from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0036097#pone.0036097-Kappeler1" target="_blank">[50]</a>, supplemented by data from other sources <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0036097#pone.0036097-Nash1" target="_blank">[51]</a>–<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0036097#pone.0036097-Weisenseel1" target="_blank">[55]</a>.</p>3<p>This is a 0-day-old <i>T. syrichta</i>. Two additional <i>T. syrichta</i> (one fetal and one 6-day-old) were studied for comparison to this 0-day-old infant. However, they were excluded from statistical analyses due to prematurity or, in the case of the 6-day-old, because the eyes had been removed prior to acquisition.</p

Relationship of Log10 eye and orbital diameters to Log10 cranial length in prosimians.

<p>The regression line is calculated from the strepsirrhines only. Thin lines indicate 95% confidence interval. Note that <i>Tarsius</i> is an outlier in each case.</p