Optic chiasm in the species of order Clupeiformes, family Clupeidae: optic chiasm of Spratelloides gracilis shows an opposite laterality to that of Etrumeus teres

Abstract

In most teleost fishes, the optic nerves decussate completely as they project to the mesencephalic region. Examination of the decussation pattern of 25 species from 11 different orders in Pisces revealed that each species shows a specific chiasmic type. In 11 species out of the 25, laterality of the chiasmic pattern was not determined; in half of the individuals examined, the left optic nerve ran dorsally to the right optic nerve, while in the other half, the right optic nerve was dorsal. In eight other species the optic nerves from both eyes branched into several bundles at the chiasmic point, and intercalated to form a complicated decussation pattern. In the present study we report our findings that Spratelloides gracilis, of the order Clupeiformes, family Clupeidae, shows a particular laterality of decussation: the left optic nerve ran dorsally to the right (n=200/202). In contrast, Etrumeus teres, of the same order and family, had a strong preference of the opposite (complementary) chiasmic pattern to that of S. gracilis (n=59/59), revealing that these two species display opposite left-right optic chiasm patterning. As far as we investigated, other species of Clupeiformes have not shown left-right preference in the decussation pattern. We conclude that the opposite laterality of the optic chiasms of these two closely related species, S. gracilis and E. teres, enables investigation of species-specific laterality in fishes of symmetric shapes.

Figure 1.

Photographs of the fish used in studies of the decussation pattern of the optic chiasm. Bars, 1 cm or 10 cm.

Figure 2.

Taxonomic classification of the fishes used and definitions of the chiasmic patterns identified in this study. (a) List of the species examined in this report. Optic chiasms were investigated in 25 species of 11 orders of freshwater and seawater fishes. (b) A type 1 chiasm is defined as a complete decussation in which the entire left optic nerve runs dorsally to the entire right optic nerve. A type 2 chiasm is that in which the entire right optic nerve runs dorsally to the entire left optic nerve (complementary to type 1 in its laterality). A type 3 chiasm is defined as that in which the optic nerves from both sides cross in a complex manner consisting of intercalated bundles. All the chiasms shown are viewed from the ventral side in Figure 2–8 except for Figure 7.

Figure 3.

Fish showing both type 1 and type 2 chiasmic patterns in equal frequencies within one species. Scientific names of the fishes are indicated in the photographs. Of the 25 species examined, 11 species showed a random preference for a type 1 or type 2 chiasm within individuals (see also Figure 4). Left column, type 1; right column, type 2.

Figure 4.

These species also displayed a random occurrence of a type 1 or type 2 chiasm (see also Figure 3).

Figure 5.

Of the 25 species examined, 7 species showed a type 3 chiasm. In these species, almost all individuals showed no laterality within the optic chiasm and the optic nerve fibres crossed in a complex manner.

Figure 6.

The optic chiasm of Spratelloides gracilis showed opposite laterality to that of Etrumeus teres, although these species belong to the same order Clupeiformes and the same family Clupeidae. (a) Optic chiasm of S. gracilis; left optic nerve invariably ran dorsally to the right optic nerve at the decussation. (b) Optic chiasm of E. teres; right optic nerve always ran dorsally to the left optic nerve.

Figure 7.

Decussation pattern within the optic chiasm of Pleuronectes herzensteini (Japanese flounder), which has a remarkably asymmetrical body. At the chiasm, the left optic nerve always ran dorsally to the right; all specimens showed definite laterality of the chiasmic pattern (n = 10/10). This figure is viewed from the dorsal side.

Figure 8.

Ancestral fishes of subclass Branchiopterygii showed a “fused” type chiasm, in which no fasciculations of the optic nerves were observed at the chiasmic point.

Figure 9.

Phylogenetic tree of the fish investigated in this report, showing the chiasmic pattern for each species. The decussation pattern in the optic chiasm is indicated by a superscript (1, 2, and 3 indicate types 1, 2, and 3 chiasm respectively; 1 & 2 indicates a mixture of types 1 and 2, occurring in equal frequency).