Photoperiodic regime influences onset of lens opacities in a non-human primate

Abstract

Background: Opacities of the lens are typical age-related phenomena which have a high influence on photoreception and consequently circadian rhythm. In mouse lemurs, a small bodied non-human primate, a high incidence (more than 50% when >seven years) of cataracts has been previously described during aging. Previous studies showed that photoperiodically induced accelerated annual rhythms alter some of mouse lemurs' life history traits. Whether a modification of photoperiod also affects the onset of age dependent lens opacities has not been investigated so far. The aim of this study was therefore to characterise the type of opacity and the mouse lemurs' age at its onset in two colonies with different photoperiodic regimen.

Methods: Two of the largest mouse lemur colonies in Europe were investigated: Colony 1 having a natural annual photoperiodic regime and Colony 2 with an induced accelerated annual cycle. A slit-lamp was used to determine opacities in the lens. Furthermore, a subset of all animals which showed no opacities in the lens nucleus in the first examination but developed first changes in the following examination were further examined to estimate the age at onset of opacities. In total, 387 animals were examined and 57 represented the subset for age at onset estimation.

Results: The first and most commonly observable opacity in the lens was nuclear sclerosis. Mouse lemurs from Colony 1 showed a delayed onset of nuclear sclerosis compared to mouse lemurs from Colony 2 (4.35 ± 1.50 years vs. 2.75 ± 0.99 years). For colony 1, the chronological age was equivalent to the number of seasonal cycles experienced by the mouse lemurs. For colony 2, in which seasonal cycles were accelerated by a factor of 1.5, mouse lemurs had experienced 4.13 ± 1.50 seasonal cycles in 2.75 ± 0.99 chronological years.

Discussion: Our study showed clear differences in age at the onset of nuclear sclerosis formation between lemurs kept under different photoperiodic regimes. Instead of measuring the chronological age, the number of seasonal cycles (N = four) experienced by a mouse lemur can be used to estimate the risk of beginning nuclear sclerosis formation. Ophthalmological examinations should be taken into account when animals older than 5-6 seasonal cycles are used for experiments in which unrestricted visual ability has to be ensured. This study is the first to assess and demonstrate the influence of annual photoperiod regime on the incidence of lens opacities in a non-human primate.

Keywords: Aging; Cataract; Mouse lemur; Nuclear sclerosis; Photoperiod; Primate.

Figure 1. Eye of a two year old mouse lemur.

This lens shows no opacities.

Figure 2. Eye of a four year old mouse lemur.

The lens shows first signs of nuclear sclerosis in the center of the lens. Additionally incipient posterior cortical cataract is visible.

Figure 3. Eye of an eight year old mouse lemur.

The lens shows immature, nuclear cataract with additional incipient anterior cortical cataract and anterior subcapsular cataract.

Figure 4. Eye of an 11 year old mouse lemur.

The lens is affected by mature cataract.

Figure 5. Age at the onset of nuclear sclerosis in mouse lemurs of two colonies with different photoperiodic cycles, measured in chronological years.

Chronological age of mouse lemurs showing first signs of nuclear sclerosis in both investigated colonies. Nuclear sclerosis is present at a significant younger age in colony 2 than colony 1 (colony 1, N = 27 animals; colony 2, N = 30 animals; P < 0.001).

Figure 6. Age at the onset of nuclear sclerosis in mouse lemurs of two colonies with different photoperiodic cycles, measured in number of seasonal cycles.

Number of seasonal cycles experienced by mouse lemurs showing first signs of nuclear sclerosis in both investigated colonies. The onset of NS does not significantly differ between both colonies (colony 1, N = 27 animals; colony 2, N = 30 animals; P = 0.671).