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

Joshua R Cummings,Susan J Rehorek,E Christopher Kirk,Magdalena N Muchlinski,Valerie B Deleon,Timothy D Smith

doi:10.1371/journal.pone.0036097

Abstract

BackgroundPrimates 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.Methodology/Principal FindingsWe 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.Conclusions/SignificanceThe 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.

Highlights

Compared to other mammals, primates tend to have large eyes relative to head or body size [1]
The second goal of this study is to investigate whether relative eye size at birth is influenced by life history or ecology
In separate bivariate plots of axial eye diameter, transverse eye diameter, and orbital aperture diameter versus cranial length (Figure 2), a close relationship is seen between cranial length and eye or orbit diameters among strepsirrhines at birth (Figure 2 includes a late fetal Loris tardigradus that falls close to the regression line)

Summary

Introduction

Primates tend to have large eyes relative to head or body size [1]. During fetal development the relatively large primate eye profoundly influences facial form, perhaps more so in small-bodied nocturnal species [8]. There is a reasonable basis to expect eyes to grow either in a ‘‘somatic’’ rate (in tandem with head or body size), or in a ‘‘neural’’ pattern (e.g., in tandem with brain development). Eye growth might instead be predicted to mirror developmental patterns observed for the brain, such as a relatively large extent of prenatal growth [11]. Primates have large eyes relative to head size, which profoundly influence the ontogenetic emergence of facial form. Growth of the primate eye is only understood in a narrow taxonomic perspective, with information biased toward anthropoids

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Conclusion