Neofunctionalization of a Duplicate<i>dachshund</i>Gene Underlies the Evolution of a Novel Leg Segment in Arachnids

Turetzek, Natascha; Pechmann, Matthias; Schomburg, Christoph; Schneider, Julia; Prpic, Nikola‐Michael

doi:10.1093/molbev/msv200

Cited by 48 publications

(64 citation statements)

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“…We have previously shown that the duplication of the dachshund gene ( dac ) is an old duplication and has apparently occurred before the diversification of the arachnid orders [17]. Our phylogenetic analysis of hth shows that in contrast to dac , the hth duplicates in scorpions and spiders are placed in separate clades in the phylogenetic tree.…”

Section: Discussionmentioning

confidence: 83%

“…phalangioides) embryos were obtained from our laboratory stocks in Göttingen, and were treated as described previously [17, 44]. For gene cloning, we used SMARTer RACE cDNA (Clontech, Mountain View, CA, USA) synthesized from a combination of all embryonic stages of the different spider species (for details see [17]). Initial fragments of Pp-hth1 and Pt-hth2 were amplified using nested PCR with degenerated primers as described in [23].…”

Section: Methodsmentioning

confidence: 99%

“…Especially in plants where duplications of the entire genome are frequent, gene duplications have been implicated in the evolution of morphological novelties [6–8]. But also in animals, gene duplications have been linked to evolutionary novelties, for example in the evolution of spermatogenesis, the immune system, protective embryonic membranes, the physiology of digestion, and the morphology of the exoskeleton in Drosophila species [9, 10], sexual dimorphism in stalk-eyed flies [11], the visual system in crustaceans and insects [12], sex determination in bees [13], electric organs and the bulbus arteriosus in fish [14, 15], or the silk producing apparatus and leg morphology in spiders [16, 17]. …”

Section: Introductionmentioning

confidence: 99%

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Rapid diversification of homothorax expression patterns after gene duplication in spiders

et al. 2017

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BackgroundGene duplications provide genetic material for the evolution of new morphological and physiological features. One copy can preserve the original gene functions while the second copy may evolve new functions (neofunctionalisation). Gene duplications may thus provide new genes involved in evolutionary novelties.ResultsWe have studied the duplicated homeobox gene homothorax (hth) in the spider species Parasteatoda tepidariorum and Pholcus phalangioides and have compared these data with previously published data from additional spider species. We show that the expression pattern of hth1 is highly conserved among spiders, consistent with the notion that this gene copy preserves the original hth functions. By contrast, hth2 has a markedly different expression profile especially in the prosomal appendages. The pattern in the pedipalps and legs consists of several segmental rings, suggesting a possible role of hth2 in limb joint development. Intriguingly, however, the hth2 pattern is much less conserved between the species than hth1 and shows a species specific pattern in each species investigated so far.ConclusionsWe hypothesise that the hth2 gene has gained a new patterning function after gene duplication, but has then undergone a second phase of diversification of its new role in the spider clade. The evolution of hth2 may thus provide an interesting example for a duplicated gene that has not only contributed to genetic diversity through neofunctionalisation, but beyond that has been able to escape evolutionary conservation after neofunctionalisation thus forming the basis for further genetic diversification.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-017-1013-0) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 83%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Rapid diversification of homothorax expression patterns after gene duplication in spiders

et al. 2017

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“…3A). Additionally, duplication of dac in spiders created a paralog, dac2, which is responsible for an additional leg segment, the patella (Turetzek et al, 2016). Mutually antagonistic interactions between the genes expressed in the proximal and medial and between medial and distal domains maintain the domain identity in the leg (Dong et al, 2001).…”

Section: Dll Regulation and Downstream Targetsmentioning

confidence: 99%

Distal-lesshomeobox genes of insects and spiders: genomic organization, function, regulation and evolution

2016

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The Distal-less (Dll) genes are homeodomain transcription factors that are present in most Metazoa and in representatives of all investigated arthropod groups. In Drosophila, the best studied insect, Dll plays an essential role in forming the proximodistal axis of the legs, antennae and analia, and in specifying antennal identity. The initiation of Dll expression in clusters of cells in mid-lateral regions of the Drosophila embryo represents the earliest genetic marker of limbs. Dll genes are involved in the development of the peripheral nervous system and sensitive organs, and they also function as master regulators of black pigmentation in some insect lineages. Here we analyze the complete genomes of six insects, the nematode Caenorhabditis elegans and Homo sapiens, as well as multiple Dll sequences available in databases in order to examine the structure and protein features of these genes. We also review the function, expression, regulation and evolution of arthropod Dll genes with emphasis on insects and spiders.

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“…Gene duplication provides raw genetic material for evolutionary adaptation (Turetzek, Pechmann, Schomburg, Schneider, & Prpic, 2016). The adaptive evolution of insects usually occurs through gene duplication events.…”

Section: Introductionmentioning

confidence: 99%

Duplication and diversification of trehalase confers evolutionary advantages on lepidopteran insects

Zhou

Katsuma

et al. 2019

Molecular Ecology

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Gene duplication provides a major source of new genes for evolutionary novelty and ecological adaptation. However, the maintenance of duplicated genes and their relevance to adaptive evolution has long been debated. Insect trehalase (Treh) plays key roles in energy metabolism, growth, and stress recovery. Here, we show that the duplication of Treh in Lepidoptera (butterflies and moths) is linked with their adaptation to various environmental stresses. Generally, two Treh genes are present in insects: Treh1 and Treh2. We report three distinct forms of Treh in lepidopteran insects, where Treh1 was duplicated into two gene clusters (Treh1a and Treh1b). These gene clusters differ in gene expression patterns, enzymatic properties, and subcellular localizations, suggesting that the enzymes probably underwent sub‐ and/or neofunctionalization in the lepidopteran insects. Interestingly, selective pressure analysis provided significant evidence of positive selection on duplicate Treh1b gene in lepidopteran insect lineages. Most positively selected sites were located in the alpha‐helical region, and several sites were close to the trehalose binding and catalytic sites. Subcellular adaptation of duplicate Treh1b driven by positive selection appears to have occurred as a result of selected changes in specific sequences, allowing for rapid reprogramming of duplicated Treh during evolution. Our results suggest that gene duplication of Treh and subsequent functional diversification could increase the survival rate of lepidopteran insects through various regulations of intracellular trehalose levels, facilitating their adaptation to diverse habitats. This study provides evidence regarding the mechanism by which gene family expansion can contribute to species adaptation through gene duplication and subsequent functional diversification.

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Neofunctionalization of a DuplicatedachshundGene Underlies the Evolution of a Novel Leg Segment in Arachnids

Cited by 48 publications

References 37 publications

Rapid diversification of homothorax expression patterns after gene duplication in spiders

Rapid diversification of homothorax expression patterns after gene duplication in spiders

Distal-lesshomeobox genes of insects and spiders: genomic organization, function, regulation and evolution

Duplication and diversification of trehalase confers evolutionary advantages on lepidopteran insects

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