Ancient pheromone blend as an alternative for copulation in internally fertilizing salamanders

Bocxlaer, Ines Van; Treer, Dag; Maex, Margo; Vandebergh, Wim; Janssenswillen, Sunita; Stegen, Gwij; Kok, Philippe J. R.; Willaert, Bert; Matthijs, Sandra; Martens, Erik; Mortier, Anneleen; Greve, Henri De; Proost, Paul; Bossuyt, Franky

doi:10.7287/peerj.preprints.457v1

Cited by 2 publications

(13 citation statements)

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“…The oldest known vertebrate sex pheromone system is the ''sodefrin precursor-like factor'' (SPF) pheromone system, a series of proteins involved in the courtship process of many salamander families (Plethodontidae, Ambystomatidae and Salamandridae) [9,[12][13][14][15][16][17]. In aquatically reproducing newts (Salamandridae), males display an underwater courtship dance in which they direct a stream of these water-soluble protein pheromones from their cloaca toward the female [18,19].…”

Section: Resultsmentioning

confidence: 99%

“…To assay the courtship pheromone function of persuasins, we first used immobilized lectins to selectively remove glycosylated SPF proteins from unglycosylated persuasins (Table S1) and obtained fractions with purified persuasins after a final, polishing RP-HPLC step (Figures S1B and S1C; see STAR Methods for details). We then adopted the same two-female test with palmate newts as previously employed for SPF to investigate the courtship pheromone function of persuasins [9]. When two receptive females (in absence of a male) are exposed to male courtship pheromones, they start showing courtship responses toward each other (including closely following the movements of the other female) that are similar to how females follow a male during courtship before spermatopohore deposition [19].…”

Section: Resultsmentioning

confidence: 99%

“…Two extant clades of SPF pheromones, termed alpha and beta, arose through an ancient gene duplication event followed by a series of additional duplications. Although earlier behavioral tests showed that a single alpha SPF is able to increase female receptivity, beta SPFs are clearly more abundant in palmate newts [9]. Here, we used anion exchange chromatography to isolate the highest expressed beta SPF protein (SPF1; Figure S1D) and subsequently investigated its receptivity-enhancing capacity in a two-female behavioral assay.…”

Section: A C B Figure 2 Evolution Of Persuasinmentioning

confidence: 98%

“…Animal sex pheromone systems often exist as multicomponent signals [1][2][3][4][5][6][7][8][9][10][11] to which chemical cues have been added over evolutionary time. Little is known on why and how additional molecules become recruited and conserved in an already functional pheromone system.…”

Section: In Briefmentioning

confidence: 99%

“…Little is known on why and how additional molecules become recruited and conserved in an already functional pheromone system. Here, we investigated the evolutionary trajectory of a series of 15 kDa proteins-termed persuasins-that were co-opted more recently alongside the ancient sodefrin precursor-like factor (SPF) courtship pheromone system in salamanders [9,12]. Expression, genomic, and molecular phylogenetic analyses show that persuasins originated from a gene that is expressed as a multidomain protein in internal organs where it has no pheromone function but underwent gene duplication and neofunctionalization.…”

Section: In Briefmentioning

confidence: 99%

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Exaptation as a Mechanism for Functional Reinforcement of an Animal Pheromone System

et al. 2018

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Animal sex pheromone systems often exist as multicomponent signals [1-11] to which chemical cues have been added over evolutionary time. Little is known on why and how additional molecules become recruited and conserved in an already functional pheromone system. Here, we investigated the evolutionary trajectory of a series of 15 kDa proteins-termed persuasins-that were co-opted more recently alongside the ancient sodefrin precursor-like factor (SPF) courtship pheromone system in salamanders [9, 12]. Expression, genomic, and molecular phylogenetic analyses show that persuasins originated from a gene that is expressed as a multi-domain protein in internal organs where it has no pheromone function but underwent gene duplication and neofunctionalization. The subsequent evolution combined domain loss and the introduction of a proteolytic cleavage site in the duplicated gene to give rise to two-domain cysteine rich proteins with structural properties similar to SPF pheromones [12]. An expression shift to the pheromone-producing glands, where expression of persuasins was immediately spatiotemporally synchronized with the already available pheromone system, completed the birth of a new pheromone. Electrostatic forces between members of both protein families likely enhance co-localization and simultaneous activation of different female olfactory neurons, explaining why persuasins immediately had a selective advantage. In line with this, behavioral assays show that persuasins increase female receptivity on their own but also exert a cumulative or synergistic effect in combination with SPF, clearly reinforcing the pheromone system as a whole. Our study reveals molecular remodeling of an existing protein architecture as an evolutionary mechanism for functional reinforcement of animal pheromone systems.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: A C B Figure 2 Evolution Of Persuasinmentioning

confidence: 98%

Section: In Briefmentioning

confidence: 99%

Section: In Briefmentioning

confidence: 99%

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Exaptation as a Mechanism for Functional Reinforcement of an Animal Pheromone System

et al. 2018

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Proteinaceous Pheromone Homologs Identified from the Cloacal Gland Transcriptome of a Male Axolotl, Ambystoma mexicanum

Hall¹,

Eisthen²,

Williams³

2016

PLoS ONE

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Pheromones play an important role in modifying vertebrate behavior, especially during courtship and mating. Courtship behavior in urodele amphibians often includes female exposure to secretions from the cloacal gland, as well as other scent glands. The first vertebrate proteinaceous pheromone discovered, the decapeptide sodefrin, is a female attracting pheromone secreted by the cloacal gland of male Cynops pyrrhogaster. Other proteinaceous pheromones in salamanders have been shown to elicit responses from females towards conspecific males. The presence and levels of expression of proteinaceous pheromones have not been identified in the family Ambystomatidae, which includes several important research models. The objective of this research was therefore to identify putative proteinaceous pheromones from male axolotls, Ambystoma mexicanum, as well as their relative expression levels. The results indicate that axolotls possess two different forms of sodefrin precursor-like factor (alpha and beta), as well as a putative ortholog of plethodontid modulating factor. The beta form of sodefrin precursor-like factor was amongst the most highly expressed transcripts within the cloacal gland. The ortholog of plethodontid modulating factor was expressed at a level equivalent to the beta sodefrin precursor-like factor. The results are from a single male axolotl; therefore, we are unable to assess how representative our results may be. Nevertheless, the presence of these highly expressed proteinaceous pheromones suggests that male axolotls use multiple chemical cues to attract female conspecifics. Behavioral assays would indicate whether the putative protein pheromones elicit courtship activity from female axolotls.

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Ancient pheromone blend as an alternative for copulation in internally fertilizing salamanders

Cited by 2 publications

References 5 publications

Exaptation as a Mechanism for Functional Reinforcement of an Animal Pheromone System

Exaptation as a Mechanism for Functional Reinforcement of an Animal Pheromone System

Proteinaceous Pheromone Homologs Identified from the Cloacal Gland Transcriptome of a Male Axolotl, Ambystoma mexicanum

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