Evolution of Color and Pattern in Etheostomatinae (Darter Fishes)

Abstract

Often directly related to non-random mating, kin recognition, predator avoidance, and other life strategies, diversification of coloration may be an important factor in evolutionary processes like speciation and adaptive radiation. Darters (Etheostomatinae) are a speciose clade of freshwater fishes belonging to family Percidae that show remarkable diversity in color and color pattern, including species with bold and complex patterns. Their high variation in coloration coupled with species richness makes Darters an excellent group for understanding the macroevolutionary and ecological factors driving the evolution of color. Using recent developments in color and pattern analysis such as recolorize in R Studio and adjacency analysis, we were able more objectively and accurately quantify darter color patterns than any prior study of this clade. Using multivariate approaches for understanding the variation in complex traits and their relationship to other factors (e.g., habitat) and phylogenetic comparative methods such as and evolutionary model fitting, we were able to quantitatively describe trends in color pattern and color diversification in this clade. Our data set was comprised of 107 species of darters and 352 photos from field sites and online databases. We found that almost 40% of color variation in Etheostomatinae can be described across the first four PC axes, which varied primarily in factors like the presence of conspicuous colors like red and blue, the complexity of color pattern, the presence of melanistic colors (blacks) and the strength of patch boundaries. Modern darter color diversity appears to have originated towards the present, rather than early in the radiation of darters. Color also seems to be evolving rapidly in younger clades such as Etheostoma and Nothonotus and is much slower in basal groups like Ammocrypta, Crystallaria, and Percina. Using canonical correspondence analysis we found trends of brighter, more conspicuous color and pattern were associated with shallow, upland streams and riffles, with more dull colors and patterns associated with lower elevation, soft substrates, large river and pool environments. Maximum likelihood model fitting also showed that small rivers and riffle environments were associated with broadly accelerated evolution in diverse color traits, with fast color evolution in large rivers being restricted to dark-light color characteristics. In addition to niche partitioning among different habitat environments (sand, rock, vegetation), color diversification could be the result of differing photic environments (light spectrum changes, water clarity, etc) and differing female preferences in sexual selection. Our results are consistent with natural selection on darter color in small river and shallow riffle environments, likely driven by changes in predator abundance and/or differences in photic conditions. Enhanced color diversification in some river habitats (streams and riffles) may indirectly contribute to reproductive isolation in darters through reinforcing sexual signaling in secondary contact between lineages. Further expansion of this data increase taxonomic coverage could help to further test for relationships between darter coloration and lineage diversification (speciation and extinction). Our work helps to understand the origins of the varied and brilliant coloration of darters and illustrates how new statistical toolkits can expand our evolutionary understanding of organismal color diversity.