The evolution of communication systems is a process whereby a relationship is established and maintained between a signal and a receiver. The evolutionary sequence of signal and reception may take one of two forms. For example, color patterns used in communication may have evolved prior to the visual acuity necessary for the detection of color. Alternatively, color vision may have evolved prior to color patterns. The sensory bias hypothesis explains the coevolution of signal and reception as the exploitation by the signaler (through color pattern) of a preexisting neural structure (color vision) in the receiver (Ryan et al. 1990). Phylogenetic distributions of retinal structures and the presence or absence of color signals is one possible test of the sensory bias hypothesis (Ryan et al. 1990; see comment by Ahlbert 1970: 447).
Fishes of the family Percidae represent an ideal group to test the sensory bias hypothesis. Percidae is the second largest family of North American freshwater fishes and consists of 5 genera with 145 described species (Burr and Mayden 1992). Darters (Crystallaria, Etheostoma, and Percina) represent the most speciose group of Percids and includes many colorful and a few monochromatic species (Table 1). Males of many darters use their bright color patterns to attract females during breeding season and to warn other males against territorial invasion (Page 1985). This use of color in communication in darters suggests that these fishes possess the ability to detect color.
Despite the bright colors of many darter species, only the visual systems of the larger percids (Stizostedion canadense, S. vitreum, and Perca flavescens) are well documented (Ahlbert 1970; Ali et al. 1977; Zyznar and Ali 1974). The retinal structure in Stizostedion and Perca is marked by the presence of abundant rods, large twin cones, and multiple layers of horizontal cells characteristic of a visual system optimized for low levels of ambient light (as opposed to visual acuity or color sensitivity).
There are ample reasons to suppose that the visual system of darters differs from that of the larger percids. First, the use of color in communication is not found in either Stizostedion or Perca. Second, darters are most active during daylight hours (Page 1983) whereas Stizostedion and Perca are most active at night and during twilight hours (Ali et al. 1977). Further, most darters occupy creeks and small streams with clear water. Such well-lit habitats are conducive to the use of color communication. However, retinal structure of darters remains undocumented and it is unknown whether darters possess the ability to detect color.
I examined the retinal structure of representative percids to determine whether a difference in color patterns coincides with visual acuity. I am now in the process of collecting sequences of the cytochrome b protein coding region for the species included in this study in order to estimate their phylogenetic relationships. I will use the phylogenetic distribution of retinal structure characters and body color characters documented herein on the DNA-based phylogeny as evidence to infer the evolutionary sequence of color vision and color communication in darters.
Histology.–All specimens included in this project were collected in their respective habitats and promptly preserved at the collection site in 10% formalin. Retinal tissue was dissected from light-adapted fish to control for light-sensitive cell migration within the retina. The formalin-fixed tissues were then dehydrated in an ethanol series and cleared in xylenes prior to embedding in paraffin. The paraffin block was sectioned (transverse sections) and the sections were mounted to slides. I stained the mounted sections with hematoxylin and counter-stained with eosin. The structure of photoreceptive cells and the relative abundance of rods and different types of cones was documented with a Leitz Ortholux microscope and Leica camera.
Phylogenetic analysis.–Sequences of the mitochondrial cytochrome b protein-coding region for many of the species included in this study are available from Genbank. I will submit PCR products from species not documented with Genbank for sequencing to Cornell University’s Biotechnology Laboratory. Sequences will be aligned with CLUSTALW (Thompson et al. 1994) and imported into the Maximum Likelihood algorithm available in PHYLIP (Felsenstein 1995). Character traits (i.e., presence/absence of cones, specific retinal structures, presence/absence of color on bodies) will be mapped onto the phylogeny under the criterion of maximum parsimony. RESULTS AND DISCUSSION
I examined the histological structure of 18 species representing the three genera of darters (Table 1). Perca flavescens and two species of Stizostedion were included to replicate the findings of previous studies (Ahlbert 1970; Ali et al. 1977; Zyznar and Ali 1974). Distinctive histological structures of Stizostedion and Perca retinae are giant twin cones (Figure 1) and three rows of stellate horizontal cells which function to increase light sensitivity by laterally linking photoreceptors (rods and cones; Ahlbert 1970; Ali et al. 1977; Zyznar and Ali 1974). Darters have smaller, more densely packed single cones and a specialized horizontal cell layer composed of cuboidal cells which form an epithelial-like sheet (Figure 2). Bipolar cells are intermediaries between photoreceptors and the ganglion cells that lead to the optic nerve. Stizostedion and Perca have a higher ratio of photoreceptors to bipolar cells than darters. The greater degree of neural convergence in Stizostedion and Perca supports the contention that these large percids are more light sensitive than the diurnal darters. We conclude that darters have a greater degree of visual acuity than the larger percids, which may be correlated with color vision.
Final completion of the phylogenetic analysis and mapping of character traits (retinal structures, body color, and temporal activity) onto the phylogeny will allow me to infer the evolutionary sequence of darter body coloration and the darters’ ability to detect body coloration. I am using the phylogenetic hypothesis proposed by Wiley (1992) until my sequence data are complete (Figure 3). Phylogenetic placement of color vision and color communication on the topology suggests that color vision predates color communication in percids. The evolution of color vision prior to color bodies supports the sensory bias hypothesis.
Ahlbert, Inga-Britt. 1970. The organization of the cone cells in the retinae of four teleosts with different feeding habits (Perca fluviatilis L., Lucioperca lucioperca L., Acerina cernua L. and Coregonus albula L.). Arkiv for Zoologi 22:445-481.
Ali, M.A., R.A. Ryder, and M. Anctil. 1977. Photoreceptors and visual pigments as related to behavioral responses and preferred habitats of Perches (Perca spp.) and Pikeperches (Stizostedion spp.). Journal of the Fisheries Research Board of Canada 34:1475-1480.
Felsenstein, J. 1995. PHYLIP: Phylogeny Inference Package, version 3.57c. University of Washington, Seattle, WA.
Page, L.M. 1983. Handbook of darters. T.F.H. Publications, Inc. Neptune City, NJ.
Page, L.M. 1985. Evolution of reproductive behaviors in percid fishes. Illinois Natural History Survey Bulletin 33:275-293.
Mayden, R.L., B.M. Burr, and R.R. Miller. 1992. Phylogenetics and North American freshwater fishes. Pp. 827-863 in R.L. Mayden (ed.) Systematics, historical ecology, and North American freshwater fishes. Stanford University Press, Stanford, CA.
Ryan, M.J. and R.C. Drews. 1990. Vocal morphology of the Physalaemus pustulosus specis group (Family Leptodactylidae): Morphological response to sexual selection for complex calls. Biological Journal of the Linnean Society 40:37-52.
Thompson, J.D., D.G. Higgins, and T.J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alighnment through sequence weighting, positions-specific gap penalties, and weight matrix choice. Nucleic Acids Research 22:4673-4680.
Wiley, E.O. 1992. Phylogenetic relationships of the Percidae (Teleostei: Perciformes): A preliminary hypothesis. Pp. 247-267 in R.L. Mayden (ed.) Systematics, historical ecology, and North American freshwater fishes. Stanford University Press, Stanford, CA.
Zyznar, E.S. and M.A. Ali. 1975. An interpretative study of the organization of the visual cells and tapetum lucidum of Stizostedion. Canadian Journal of Zoology 53:180-196.
Table 1. Presence (1) or absence (0) of specific body colors, retinal optimization as
determined by retinal structures (A=optimized for acuity, S=optimized for light sensitivity), and
periods of peak activity (D=diurnal, T=twilight, N=nocturnal, and ?=undocumented) in percids
Figure 1. Section of neural retinal from Stizostedion vitreum. Note large cones and abundant rod nuclei.
Figure 2. Section through neural retina of Etheostoma blennioides. Note approximately equal number of rod nuclei and cone ellipsoids.
Figure 3. Hypothesized phylogenetic relationships among percid genera (after Wiley 1992). Green bar indicates origin of color vision, blue bar indicates origin of color communication.