Rods and cones in an enantiornithine bird eye from the Early Cretaceous Jehol Biota

Abstract

Extant birds have an extensive spectral range of colour vision among vertebrates, but evidence of colour vision among extinct birds has hitherto been lacking. An exceptionally well-preserved extinct enantiornithine fossil bird from the Early Cretaceous Jiufotang Formation (120 Ma) of Liaoning, China, provides the first report of mineralised soft tissue of a bird eye. Cone cells are identified, which have preserved oil droplets falling between wide ranges of size that can be compared with an extant house sparrow. The size distribution of oil droplets of extant birds demonstrates good correlation between size and the detectable wavelength range of the cone cells: UV-sensitive cones contain the smallest oil droplets, while red-sensitive cones possess the largest. The data suggests that this Early Cretaceous bird could have possessed colour vision.

Keywords: Biological sciences; Evolution; Palaeobiology.

Fig. 1

An enantiornithine bird from the Jiufotang Formation, Early Cretaceous, Liaoning, China (a–f) and retina of an extant house sparrow Passer domesticus (g,h). (a) Completely preserved specimen (SNHM: 6105). (b) Enlarged eye region of (a) showing eye orbit within the white dotted line, black material (white arrow) and sample point (yellow arrow) of the fragment of (c). (c) Digital microphotograph of an eye fragment. (d) SEM image of an eye fragment. (e) SEM of cone and rod cells with their oil droplets. (f) Labelled image of (e) showing position of oil droplets (red circles), cone (blue solid line) and rod (yellow solid line) cells. (g) SEM image of rods (yellow solid line), cones (blue solid line) and oil droplets (red circles). (h) Transmitted microphotograph of oil droplets. Scale bars: a = 2 cm; b = 5 mm; c,d = 100 μm; e–h = 10 μm.

Fig. 2

SEM images of the retinas of an Early Cretaceous enantiornithine bird and an extant house sparrow Passer domesticus. (a) A fragment of the retina of the fossil bird preserving many oil droplets (o) in the upper left region of the broken line, pigment epithelium (p), and rods (r) and cones (c). (b) Magnified image of (a) showing oil droplets (red circles) and pigment epithelium (p), and rods (yellow solid line) and cones (blue solid line). (c) A fragment of the fossil pigment epithelium (p) with preserved fine fibrous structures. (d) An enlargement of the fossil pigment epithelium containing elongate melanosomes (m). (e) Transverse section of the retina of an extant house sparrow. The retina is composed of pigment epithelium (p), cones (c) and rods (r) with oil droplets, an outer nuclear layer (on), and an inner nuclear layer (in) oriented in the proximal-distal plane of the eyeball. (f) A fragment of the retina of an extant house sparrow. Many oil droplets (red circles) were removed from cones. (g) Pigment epithelium (p) of an extant house sparrow. (h) An enlargement of pigment epithelium of an extant house sparrow containing elongate melanosomes (m). Scale bars: a, e = 50 μm; b–d, f–h = 10 μm.

Fig. 3

Unlabelled (a, c) and labelled (b, d) SEM images of an Early Cretaceous enantiornithine bird and an extant house sparrow Passer domesticus. (a, b) A fragment of the retina of the fossil bird. (c, d) A freeze dried fragment of the retina of the house sparrow. Labelled images indicate rods (yellow solid line), cones (blue solid line) and oil droplets (red circles). Scale bar = 10 μm.

Fig. 4

SEM images of the retinas of an Early Cretaceous enantiornithine bird and a natural dried extant house sparrow Passer domesticus. (a) A fragment of the retina of the fossil bird preserving many oil droplets (o) in the upper left region, pigment epithelium (p), and rods (c) and cones (c). (b) Enlarged image of (a) showing oil droplets (red circles), pigment epithelium (p), and rods (yellow solid line) and cones (blue solid line). (c) A fragment of the fossil pigment epithelium (p) with preserved fine fibrous structures. (d) An enlargement of the fossil pigment epithelium containing elongate melanosomes (m). (e) The photosensitive organ of an extant house sparrow that is composed of cones (blue solid line) and rods (yellow solid line) with oil droplets (red circles). (f) An enlargement of (e). Oil droplets (red circles) and cone and rods (c & r) are rather flattened but associated with each other. (g) Pigment epithelium (p) of an extant house sparrow. (h) An enlargement of pigment epithelium (p) of an extant house sparrow containing elongate melanosomes. Melanosomes (m) are distinguished from bacteria (b) by their longer shape. Scale bars: a, e = 50 μm; b–d, f–h = 10 μm.

Fig. 5

A fragment of fossil retina of an Early Cretaceous enantiornithine bird and the distribution of elements within. (a) Digital microphotographs of a retinal region. (b,c) Enlargement of an area observed by laser microscope (b) and SEM (c). (d) Backscattered electron image of (a). (e–i) Distribution of the elements P, Ca, Mn, Fe, and K.

Fig. 6

Frequency distribution of area of oil droplets of an extant house sparrow Passer domesticus. (a) Histogram of all oil droplet sizes. (b–f) Histogram of sizes for each type of coloured oil droplet: clear (b), light blue (c), yellow (d), dark green (e), and red (f) (these are correlated with ultraviolet sensitive single cones [UVS], short-wavelength sensitive single cones [SWS], medium-wavelength sensitive single cones [MWS], intermediate sensitive double cones [IWS], and long-wavelength sensitive single cones [LWS], respectively). SD = Standard deviation, CI = Confidence interval.

Fig. 7

Frequency distribution of area of oil droplets of an extant Japanese quail Coturnix japonica. (a) Histogram of all oil droplet size. (b–f) Histogram of sizes for each type of coloured oil droplet: clear (b), light blue (c), yellow (d), dark green (e), and red (f) (these are correlated with ultraviolet sensitive single cones [UVS], short-wavelength sensitive single cones [SWS], medium-wavelength sensitive single cones [MWS], unknown sensitive single cones [UWS], intermediate sensitive double cones [IWS], and long-wavelength sensitive single cones [LWS], respectively). SD = Standard deviation, CI = Confidence interval.

Fig. 8

Frequency distribution of the maximum projected area of oil droplets of an Early Cretaceous enantiornithine bird and the range of each oil droplet size in an extant house sparrow. (a) Histogram of fossil oil droplet size based on Table 1. (b) Box-and-whisker diagrams of extant oil droplets size of house sparrow drawn from Fig. 6 and Table 2. The violet, light blue, green, gray, and red ranges correlate with ultraviolet sensitive single cones [UVS], short- wavelength sensitive single cones [SWS], medium-wavelength sensitive single cones [MWS], intermediate sensitive double cones [IWS], and long-wavelength sensitive single cones [LWS], respectively.

Fig. 9

Elemental spectral patterns of three points of a fragment of fossil retina of an Early Cretaceous enantiornithine bird and the distribution of elements. (a,b) Spectral patterns from retinal region (black coloured area). (c) Spectral patterns from bone region (light-yellow coloured area).

Fig. 10

Frequency distribution of the cross-sectional area of oil droplets of a Cretaceous enantiornithine bird. (a) Histogram of oil droplet size. (b) Kernel density estimation of (a). (c) Result of number of modes (k) and p-values.

Fig. 11

Frequency distribution of the cross-sectional area of oil droplets of an extant house sparrow Passer domesticus. (a) Histogram of oil droplet size. (b) Kernel density estimation of (a). (c) Result of number of modes (k) and p-values.

Fig. 12

Frequency distribution of the cross-sectional area of oil droplets of an extant Ural owl Strix uralensis. (a) Histogram of oil droplet size. (b) Kernel density estimation of (a). (c) Result of number of modes (k) and p-values.