Abstract
BackgroundTo understand the evolutionary significance of female mate choice for colorful male ornamentation, the underlying regulatory mechanisms of such ornamentation must be understood for examining how the ornaments are associated with “male qualities” that increase the fitness or sexual attractiveness of offspring. In the guppy (Poecilia reticulata), an established model system for research on sexual selection, females prefer males possessing larger and more highly saturated orange spots as potential mates. Although previous studies have identified some chromosome regions and genes associated with orange spot formation, the regulation and involvement of these genetic elements in orange spot formation have not been elucidated. In this study, the expression patterns of genes specific to orange spots and certain color developmental stages were investigated using RNA-seq to reveal the genetic basis of orange spot formation.ResultsComparing the gene expression levels of male guppy skin with orange spots (orange skin) with those without any color spots (dull skin) from the same individuals identified 1102 differentially expressed genes (DEGs), including 630 upregulated genes and 472 downregulated genes in the orange skin. Additionally, the gene expression levels of the whole trunk skin were compared among the three developmental stages and 2247 genes were identified as DEGs according to color development. These analyses indicated that secondary differentiation of xanthophores may affect orange spot formation.ConclusionsThe results suggested that orange spots might be formed by secondary differentiation, rather than de novo generation, of xanthophores, which is induced by Csf1 and thyroid hormone signaling pathways. Furthermore, we suggested candidate genes associated with the areas and saturation levels of orange spots, which are both believed to be important for female mate choice and independently regulated. This study provides insights into the genetic and cellular regulatory mechanisms underlying orange spot formation, which would help to elucidate how these processes are evolutionarily maintained as ornamental traits relevant to sexual selection.
Highlights
To understand the evolutionary significance of female mate choice for colorful male ornamentation, the underlying regulatory mechanisms of such ornamentation must be understood for examining how the ornaments are associated with “male qualities” that increase the fitness or sexual attractiveness of offspring
The following criteria were used to differentiate the three stages of color development for later experiments: stage 1 was defined as the period from the start of gonopodia formation before the emergence of male-specific body coloration, whereas stage 2 was defined as the start of orange spot formation, and stage 3 was defined as the completion of body coloration at approximately 3–4 weeks after stage 2 (Fig. 2, Additional file 1)
The results of the present study suggest that secondary differentiation of larval cryptic xanthophores into adult pigmented xanthophores occurs during orange spot formation, which is induced by Csf1 and thyroid hormone (TH) signaling [39, 40] (Fig. 3), and genes involved in these signaling pathways might include a regulator of the areas of orange spots functioning in female mate choice
Summary
To understand the evolutionary significance of female mate choice for colorful male ornamentation, the underlying regulatory mechanisms of such ornamentation must be understood for examining how the ornaments are associated with “male qualities” that increase the fitness or sexual attractiveness of offspring. In the guppy (Poecilia reticulata), an established model system for research on sexual selection, females prefer males possessing larger and more highly saturated orange spots as potential mates. As a typical example of sexual dimorphism, male guppies have vivid color spots and are believed to be the most color-polymorphic vertebrates [8] Females choose their mates based on various characteristics and Kawamoto et al BMC Ecology and Evolution (2021) 21:211 tend to prefer males with larger and more highly saturated orange spots [10, 11]
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