Rapid evolution of the visual system: a cellular assay of the retina and dorsal lateral geniculate nucleus of the Spanish wildcat and the domestic cat

Abstract

The large Spanish wildcat, Felis silvestris tartessia, has retained features of the Pleistocene ancestor of the modern domestic cat, F. catus. To gauge the direction and magnitude of short-term evolutionary change in this lineage, we have compared the retina, the optic nerve, and the dorsal lateral geniculate nucleus (LGN) of Spanish wildcats and their domestic relatives. Retinas of the two species have the same area. However, densities of cone photoreceptors are higher in wildcat--over 100% higher in the area centralis--whereas rod densities are as high, or higher, in the domestic lineage. Densities of retinal ganglion cells are typically 20-100% higher across the wildcat retina, and the total ganglion cell population is nearly 70% higher than in the domestic cat. These differences are confined to the populations of beta and gamma retinal ganglion cells. In contrast, the population of alpha cells is almost precisely the same in both species. The wildcat LGN is much larger than that of the domestic cat and contains approximately 50% more neurons. However, cell size does not differ appreciably in either the retina or LGN of these species. The differences in total numbers of ganglion cells and LGN neurons correspond neatly to the overall decline in brain size in the domestic lineage and to allometric predictions based on average species differences in body size. We suggest that an increase in the severity of naturally occurring cell death is the most plausible mechanism that can account for the rapid evolutionary reduction in cell populations in this feline lineage.

Adaptive features of aquatic mammals' eye

“…The shape and position of the highdensity area in the retina indicates its close similarity to the area centralis of terrestrial carnivores (Stone, 1983;Peichl, 1992;Williams et al, 1993). The cell density in this area of all studied pinnipeds (1,000-2,500 cells/mm 2 ) is several times lower than that in some terrestrial carnivores: for example, approximately 7,000-10,000 cells/mm 2 in the domestic cat (Stone, 1983;Wong and Hughes, 1987;Williams et al, 1993), and up to 6,000-14,000 cells/mm 2 in the dog and wolf (Peichl, 1992). However, because of the much larger size of the eyeball in pinnipeds, the cell density per angular unit of the visual field is of the same order as in terrestrial carnivores, 200-400 cells/deg 2 .…”

Brain evolution and development: adaptation, allometry and constraint

“…Domesticated brains also show divergence in brain structure, with differential contraction and sometimes expansion of individual brain components [31]. The expansion of the hippocampus in homing pigeons (Columbia livia) [37] and selective decrease in the size of the lateral geniculate nucleus of domestic cats compared with Spanish wildcats [38] provide notable examples.…”

Functional Consequences of Neuronal Divergence Within the Retinogeniculate Pathway

“…However, our estimates are limited by the accuracy of current retinal ganglion cell counts. Whereas the numbers of geniculate cells seem to be quite consistent across individual cats [503,000 in Williams et al (1993); 557,000 in Madarasz et al (1978)], the number of retinal ganglion cells can vary by a factor Ͼ2 [90,000 -128,000 in Stone (1965) and Stone and Campion (1978); 150,000 in Illing and Wassle (1981); and 170,000 -240,000 in Hughes (1975Hughes ( , 1981]. Taken into account this important limitation, if we assume that our animals had 90,000 -128,000 retinal ganglion cells (Stone 1965;Stone and Campion 1978), 5% Y and 50% X (Wassle and Boycott 1991), and that the X/Y ratio across the entire dLGN was 5 (Humphrey and Murthy 1999;Mastronarde 1992;So and Shapley 1979), then the average retinogeniculate convergence would be roughly 2-3 for X A and Y A cells and 4 -5 for Y C cells.…”