Pigment pattern morphospace of Danio fishes: evolutionary diversification and mutational effects.
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ABSTRACT:
SUBMITTER: McCluskey BM
PROVIDER: S-EPMC8487636 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Fishes of the genus Danio exhibit diverse pigment patterns that serve as useful models for understanding the genes and cell behaviors underlying the evolution of adult form. Among these species, zebrafish D. rerio exhibit several dark stripes of melanophores with sparse iridophores that alternate with light interstripes of dense iridophores and xanthophores. By contrast, the closely related species D. nigrofasciatus has an attenuated pattern with fewer melanophores, stripes and interstripes. Here we demonstrate species differences in iridophore development that presage the fully formed patterns. Using genetic and transgenic approaches we identify the secreted peptide Endothelin-3 (Edn3)-a known melanogenic factor of tetrapods-as contributing to reduced iridophore proliferation and fewer stripes and interstripes in D. nigrofasciatus. We further show the locus encoding this factor is expressed at lower levels in D. nigrofasciatus owing to cis-regulatory differences between species. Finally, we show that functions of two paralogous loci encoding Edn3 have been partitioned between skin and non-skin iridophores. Our findings reveal genetic and cellular mechanisms contributing to pattern differences between these species and suggest a model for evolutionary changes in Edn3 requirements for pigment patterning and its diversification across vertebrates.
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Project description:Color patterns in African cichlid fishes vary spectacularly. Although phylogenetic analysis showed already 30 years ago that many color patterns evolved repeatedly in these adaptive radiations, only recently have we begun to understand the genomic basis of color variation. Horizontal stripe patterns evolved and were lost several times independently across the adaptive radiations of Lake Victoria, Malawi, and Tanganyika and regulatory evolution of agouti-related peptide 2 (agrp2/asip2b) has been linked to this phenotypically labile trait. Here, we asked whether the agrp2 locus exhibits particular characteristics that facilitate divergence in color patterns. Based on comparative genomic analyses, we discovered several recent duplications, insertions, and deletions. Interestingly, one of these events resulted in a tandem duplication of the last exon of agrp2. The duplication likely precedes the East African radiations that started 8-12 Ma, is not fixed within any of the radiations, and is found to vary even within some species. Moreover, we also observed variation in copy number (two to five copies) and secondary loss of the duplication, illustrating a surprising dynamic at this locus that possibly promoted functional divergence of agrp2. Our work suggests that such instances of exon duplications are a neglected mechanism potentially involved in the repeated evolution and diversification that deserves more attention.
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Project description:The Southern Ocean around Antarctica is among the most rapidly warming regions on Earth, but has experienced episodic climate change during the past 40 million years. It remains unclear how ancient periods of climate change have shaped Antarctic biodiversity. The origin of antifreeze glycoproteins (AFGPs) in Antarctic notothenioid fishes has become a classic example of how the evolution of a key innovation in response to climate change can drive adaptive radiation. By using a time-calibrated molecular phylogeny of notothenioids and reconstructed paleoclimate, we demonstrate that the origin of AFGP occurred between 42 and 22 Ma, which includes a period of global cooling approximately 35 Ma. However, the most species-rich lineages diversified and evolved significant ecological differences at least 10 million years after the origin of AFGPs, during a second cooling event in the Late Miocene (11.6-5.3 Ma). This pattern indicates that AFGP was not the sole trigger of the notothenioid adaptive radiation. Instead, the bulk of the species richness and ecological diversity originated during the Late Miocene and into the Early Pliocene, a time coincident with the origin of polar conditions and increased ice activity in the Southern Ocean. Our results challenge the current understanding of the evolution of Antarctic notothenioids suggesting that the ecological opportunity that underlies this adaptive radiation is not linked to a single trait, but rather to a combination of freeze avoidance offered by AFGPs and subsequent exploitation of new habitats and open niches created by increased glacial and ice sheet activity.
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Project description:Embryonic cell cycles of amphibians are rapid and lack zygotic transcription and checkpoint control. At the mid-blastula transition, zygotic transcription is initiated and cell divisions become asynchronous. Several cell cycle-related amphibian genes retain 2 distinct forms, maternal and zygotic, but little is known about the functional differences between these 2 forms of proteins. The minichromosome maintenance (MCM) 2-7 complex, consisting of 6 MCM proteins, plays a central role in the regulation of eukaryotic DNA replication. Almost all eukaryotes retain just a single MCM gene for each subunit. Here we report that Xenopus and zebrafish have 2 copies of MCM3 genes, one of which shows a maternal and the other a zygotic expression pattern. Phylogenetic analysis shows that the Xenopus and zebrafish zygotic MCM3 genes are more similar to their mammalian MCM3 ortholog, suggesting that maternal MCM3 was lost during evolution in most vertebrate lineages. Maternal MCM3 proteins in these 2 species are functionally different from zygotic MCM3 proteins because zygotic, but not maternal, MCM3 possesses an active nuclear localization signal in its C-terminal region, such as mammalian MCM3 orthologs do. mRNA injection experiments in zebrafish embryos show that overexpression of maternal MCM3 impairs proliferation and causes developmental defects, whereas zygotic MCM3 has a much weaker effect. This difference is brought about by the difference in their C-terminal regions, which contain putative nuclear localization signals; swapping the C-terminal region between maternal and zygotic genes diminishes the developmental defects. This study suggests that evolutionary diversification has occurred in MCM3 genes, leading to distinct functions, possibly as an adaption to the rapid DNA replication required for early development of Xenopus and zebrafish.
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Project description:The genetic basis of morphological variation provides a major topic in evolutionary developmental biology. Fish of the genus Danio display colour patterns ranging from horizontal stripes, to vertical bars or spots. Stripe formation in zebrafish, Danio rerio, is a self-organizing process based on cell-contact mediated interactions between three types of chromatophores with a leading role of iridophores. Here we investigate genes known to regulate chromatophore interactions in zebrafish that might have evolved to produce a pattern of vertical bars in its sibling species, Danio aesculapii. Mutant D. aesculapii indicate a lower complexity in chromatophore interactions and a minor role of iridophores in patterning. Reciprocal hemizygosity tests identify the potassium channel gene obelix/Kcnj13 as evolved between the two species. Complementation tests suggest evolutionary change through divergence in Kcnj13 function in two additional Danio species. Thus, our results point towards repeated and independent evolution of this gene during colour pattern diversification.
| S-EPMC7718271 | biostudies-literature
Project description:Fishes have diverse pigment patterns, yet mechanisms of pattern evolution remain poorly understood. In zebrafish, Danio rerio, pigment-cell autonomous interactions generate dark stripes of melanophores that alternate with light interstripes of xanthophores and iridophores. Here, we identify mechanisms underlying the evolution of a uniform pattern in D. albolineatus in which all three pigment cell classes are intermingled. We show that in this species xanthophores differentiate precociously over a wider area, and that cis regulatory evolution has increased expression of xanthogenic Colony Stimulating Factor-1 (Csf1). Expressing Csf1 similarly in D. rerio has cascading effects, driving the intermingling of all three pigment cell classes and resulting in the loss of stripes, as in D. albolineatus. Our results identify novel mechanisms of pattern development and illustrate how pattern diversity can be generated when a core network of pigment-cell autonomous interactions is coupled with changes in pigment cell differentiation.
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Project description:BackgroundMajor modifications to the pharyngeal jaw apparatus are widely regarded as a recurring evolutionary key innovation that has enabled adaptive radiation in many species-rich clades of percomorph fishes. However one of the central predictions of this hypothesis, that the acquisition of a modified pharyngeal jaw apparatus will be positively correlated with explosive lineage diversification, has never been tested. We applied comparative methods to a new time-calibrated phylogeny of labrid fishes to test whether diversification rates shifted at two scales where major pharyngeal jaw innovations have evolved: across all of Labridae and within the subclade of parrotfishes.ResultsDiversification patterns within early labrids did not reflect rapid initial radiation. Much of modern labrid diversity stems from two recent rapid diversification events; one within julidine fishes and the other with the origin of the most species-rich clade of reef-associated parrotfishes. A secondary pharyngeal jaw innovation was correlated with rapid diversification within the parrotfishes. However diversification rate shifts within parrotfishes are more strongly correlated with the evolution of extreme dichromatism than with pharyngeal jaw modifications.ConclusionThe temporal lag between pharyngeal jaw modifications and changes in diversification rates casts doubt on the key innovation hypothesis as a simple explanation for much of the richness seen in labrids and scarines. Although the possession of a secondarily modified PJA was correlated with increased diversification rates, this pattern is better explained by the evolution of extreme dichromatism (and other social and behavioral characters relating to sexual selection) within Scarus and Chlorurus. The PJA-innovation hypothesis also fails to explain the most dominant aspect of labrid lineage diversification, the radiation of the julidines. We suggest that pharyngeal jaws might have played a more important role in enabling morphological evolution of the feeding apparatus in labrids and scarines rather than in accelerating lineage diversification.
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Project description:Tropical reef fishes are widely regarded as being perhaps the most morphologically diverse vertebrate assemblage on earth, yet much remains to be discovered about the scope and patterns of this diversity. We created a morphospace of 2,939 species spanning 56 families of tropical Indo-Pacific reef fishes and established the primary axes of body shape variation, the phylogenetic consistency of these patterns, and whether dominant patterns of shape change can be accomplished by diverse underlying changes. Principal component analysis showed a major axis of shape variation that contrasts deep-bodied species with slender, elongate forms. Furthermore, using custom methods to compare the elongation vector (axis that maximizes elongation deformation) and the main vector of shape variation (first principal component) for each family in the morphospace, we showed that two thirds of the families diversify along an axis of body elongation. Finally, a comparative analysis using a principal coordinate analysis based on the angles among first principal component vectors of each family shape showed that families accomplish changes in elongation with a wide range of underlying modifications. Some groups such as Pomacentridae and Lethrinidae undergo decreases in body depth with proportional increases in all body regions, while other families show disproportionate changes in the length of the head (e.g., Labridae), the trunk or caudal region in all combinations (e.g., Pempheridae and Pinguipedidae). In conclusion, we found that evolutionary changes in body shape along an axis of elongation dominates diversification in reef fishes. Changes in shape on this axis are thought to have immediate implications for swimming performance, defense from gape limited predators, suction feeding performance and access to some highly specialized habitats. The morphological modifications that underlie changes in elongation are highly diverse, suggesting a role for a range of developmental processes and functional consequences.
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