The developmental and genetic trajectory of coloration in the guppy (Poecilia reticulata)

Abstract

Examining the association between trait variation and development is crucial for understanding the evolution of phenotypic differences. Male guppy ornamental caudal fin coloration is one trait that shows a striking degree of variation within and between guppy populations. Males initially have no caudal fin coloration, then gradually develop it as they reach sexual maturity. For males, there is a trade-off between female preference for caudal fin coloration and increased visibility to predators. This trade-off may reach unique endpoints in males from different predation regimes. Caudal fin coloration includes black melanin, orange/yellow pteridines or carotenoids, and shimmering iridescence. This study examined the phenotypic trajectory and genetics associated with color development. We found that black coloration always developed first, followed by orange/yellow, then iridescence. The ordering and timing of color appearance was the same regardless of predation regime. The increased expression of melanin synthesis genes correlated well with the visual appearance of black coloration, but there was no correlation between carotenoids or pteridine synthesis gene expression and the appearance of orange/yellow. The lack of orange/yellow coloration in earlier male caudal fin developmental stages may be due to reduced expression of genes underlying the development of orange/yellow xanthophores.

Sex-biased expression between guppies varying in the presence of ornamental coloration

“…More than half of the differentially expressed genes (6/10) had functions related to melanin and all melanin synthesis genes, regardless of differential expression status, were more highly expressed in males. This agrees with our hypothesis that melanin genes would exhibit more sex-bias than pteridines or carotenoids because we sampled the fish at a stage when the melanin was visually appearing and melanin synthesis gene expression is known to increase ( Dick et al., in press ).…”

“…Male caudal fins were sampled at a time when their anal fins were morphing into the gonopodium, which also correlated with early development of caudal fin coloration. This time was chosen because we found in an earlier study that males at this stage expressed the highest number of detectable color genes and it was simpler to obtain fish approximately the same age while their anal fins were still in the process of morphing ( Dick et al., in press ). Female fins were also collected, although females lack an independent marker of maturation.…”

“…Samples were stored at −80 °C until RNA extraction. The two male samples are the same as obtained during a developmental series study ( Dick et al., in press ). These two samples were taken at an early developing color stage (called stage 2), where usually just black melanin was present.…”

Convergent evolution of coloration in experimental introductions of the guppy (Poecilia reticulata)

“…Gordon did find that orange/yellow coloration had a genetic component in the common garden, but such genetic changes were not detected here. A previous study (Dick, Arendt, Reznick, & Hayashi, in review) found that genes underlying orange/yellow coloration are most differentially expressed at an earlier developmental stage (when there is no visible color), so it is possible that the fish stage sampled here (developing coloration) was too advanced to detect gene expression differences in that coloration.…”

Variation on a theme: pigmentation variants and mutants of anemonefish

“…All three chromatophore subtypes are affected when genes required for normal development of neural crest derivatives are mutated, such as mutations of Sox10 ( SRY-related HMG-box 10 ). The corresponding zebrafish mutant is called “colorless” [ 23 ] and the same gene is also required for chromatophore development in guppies [ 12 ]. To the best of our knowledge, no anemonefish lacking all three chromatophore subtypes has yet been found.…”