RESUMEN
Many animals exchange chemicals during courtship and mating. In some amphibians, sexual chemical communication is mediated by pheromones produced in male breeding glands that are transferred to the female's nostrils during mating. This has been mostly studied in salamanders, despite frogs having similar glands and courtship behaviours suggestive of chemical communication. In Neotropical poison frogs (Dendrobatidae and Aromobatidae), males of many species develop breeding glands in their fingers, causing certain fingers to visibly swell. Many also engage in cephalic amplexus, whereby the male's swollen fingers are placed in close contact with the female's nares during courtship. Here, we investigate the possible roles of swollen fingers in pheromone production using whole-transcriptome sequencing (RNAseq). We examined differential gene expression in the swollen versus non-swollen fingers and toes of two dendrobatid species, Leucostethus brachistriatus and Epipedobates anthonyi, both of which have specialised mucous glands in finger IV, the latter of which has cephalic amplexus. The overwhelming pattern of gene expression in both species was strong upregulation of sodefrin precursor-like factors (SPFs) in swollen fingers, a well-known pheromone system in salamanders. The differentially expressed SPF transcripts in each species were very high (>40), suggesting a high abundance of putative protein pheromones in both species. Overall, the high expression of SPFs in the swollen fingers in both species, combined with cephalic amplexus, supports the hypothesis that these traits, widespread across members of the subfamilies Colostethinae and Hyloxalinae (ca. 141 species), are involved in chemical signalling during courtship.
Muchos animales intercambian sustancias químicas durante el cortejo y el apareamiento. En algunos anfibios, la comunicación química sexual está mediada por feromonas producidas en las glándulas reproductoras de los machos que se transfieren a las hembras durante el apareamiento. Esto se ha estudiado sobre todo en salamandras, a pesar de que las ranas tienen glándulas similares y comportamientos de cortejo que sugieren una comunicación química. En las ranas venenosas neotropicales (Dendrobatidae y Aromobatidae), los machos de muchas especies desarrollan glándulas en los dedos, lo que hace que algunos dedos se vean hinchados. Asimismo, varias especies presentan amplexo cefálico, comportamiento de cortejo en el cual los dedos hinchados entran en estrecho contacto con las narinas y boca de la hembra. En este estudio investigamos las posibles funciones de los dedos hinchados en la producción de feromonas mediante la secuenciación del transcriptoma completo (RNAseq). Examinamos la expresión génica diferencial en los dedos hinchados y no hinchados de dos especies de dendrobátidos, Leucostethus brachistriatus y Epipedobates anthonyi, ambos con glándulas mucosas especializadas en el dedo IV, y esta última especie, con amplexo cefálico. El patrón abrumador de expresión génica en ambas especies fue la alta expression de Sodefrin PrecursorLike Factor (SPF) en los dedos hinchados, un sistema de feromonas ampliamente conocido en las salamandras. El número de transcritos SPF expresados diferencialmente en cada especie fue muy elevado (>40), lo que sugiere una gran abundancia de feromonas proteicas putativas en ambas especies. En general, la elevada expresión de SPF en los dedos hinchados en ambas especies, combinada con el amplexo cefálico, apoya la hipótesis de que estos rasgos, muy extendidos entre los miembros de las subfamilias Colostethinae e Hyloxalinae (aprox 141 especies), están implicados en la señalización química durante el cortejo.
Asunto(s)
Anuros , Transcriptoma , Animales , Masculino , Anuros/genética , Femenino , Conducta Sexual Animal/fisiología , Feromonas/genética , Atractivos Sexuales/genéticaRESUMEN
Convergent evolution is defined as the independent evolution of similar phenotypes in different lineages. Its existence underscores the importance of external selection pressures in evolutionary history, revealing how functionally similar adaptations can evolve in response to persistent ecological challenges through a diversity of evolutionary routes. However, many examples of convergence, particularly among closely related species, involve parallel changes in the same genes or developmental pathways, raising the possibility that homology at deeper mechanistic levels is an important facilitator of phenotypic convergence. Using the genus Ranitomeya, a young, color-diverse radiation of Neotropical poison frogs, we set out to 1) provide a phylogenetic framework for this group, 2) leverage this framework to determine if color phenotypes are convergent, and 3) to characterize the underlying coloration mechanisms to test whether color convergence occurred through the same or different physical mechanisms. We generated a phylogeny for Ranitomeya using ultraconserved elements and investigated the physical mechanisms underlying bright coloration, focusing on skin pigments. Using phylogenetic comparative methods, we identified several instances of color convergence, involving several gains and losses of carotenoid and pterin pigments. We also found a compelling example of nonparallel convergence, where, in one lineage, red coloration evolved through the red pterin pigment drosopterin, and in another lineage through red ketocarotenoids. Additionally, in another lineage, "reddish" coloration evolved predominantly through structural color mechanisms. Our study demonstrates that, even within a radiation of closely related species, convergent evolution can occur through both parallel and nonparallel mechanisms, challenging the assumption that similar phenotypes among close relatives evolve through the same mechanisms.
Asunto(s)
Ranas Venenosas , Venenos , Animales , Filogenia , Pigmentación/genética , Anuros , Pterinas/metabolismo , Evolución BiológicaRESUMEN
Parenting is considered a key evolutionary innovation that contributed to the diversification and expansion of vertebrates. However, we know little about how such diversity evolved. Amphibians are an ideal group in which to identify the ecological factors that have facilitated or constrained the evolution of different forms of parental care. Among, but also within, the three amphibian orders-Anura, Caudata, and Gymnophiona-there is a high level of variation in habitat use, fertilization mode, mating systems, and parental sex roles. Recent work using broad phylogenetic, experimental, and physiological approaches has helped to uncover the factors that have selected for the evolution of care and transitions between different forms of parenting. Here, we highlight the exceptional diversity of amphibian parental care, emphasize the unique opportunities this group offers for addressing key questions about the evolution of parenting, and give insights into promising novel directions of research.
RESUMEN
Poison frogs sequester alkaloid defenses from a diet of largely mites and ants. As a result, frogs are defended against certain predators and microbial infections. Frogs in the genus Oophaga exhibit complex maternal care, wherein mothers transport recently hatched tadpoles to nursery pools and return regularly to supply developing tadpoles with unfertilized (nutritive) eggs. Developing tadpoles are obligate egg feeders. Further, female O. pumilio and O. sylvatica maternally provision their nutritive eggs with alkaloid defenses, providing protection to their developing tadpoles at a vulnerable life-stage. In another genus of poison frog, Ranitomeya, tadpoles only receive and consume eggs facultatively, and it is currently unknown if mothers also provision these eggs (and thus their tadpoles) with alkaloid defenses. Here, we provide evidence that mother frogs of another species in the genus Oophaga (Oophaga granulifera) also provision alkaloid defenses to their tadpoles. We also provide evidence that Ranitomeya imitator and R. variabilis eggs and tadpoles do not contain alkaloids, suggesting that mother frogs in this genus do not provision alkaloid defenses to their offspring. Our findings suggest that among dendrobatid poison frogs, maternal provisioning of alkaloids may be restricted to the obligate egg-feeding members of Oophaga.
Asunto(s)
Alcaloides , Hormigas , Venenos , Animales , Femenino , Anuros , LarvaRESUMEN
The extent of male mate choosiness is driven by a trade-off between various environmental factors associated with the costs of mate acquisition, quality assessment and opportunity costs. Our knowledge about natural variation in male mate choosiness across different populations of the same species, however, remains limited. In this study, we compared male mate choosiness across 10 natural populations of the freshwater amphipod Gammarus roeselii (Gervais 1835), a species with overall high male mating investments, and evaluated the relative influence of population density and sex ratio (both affecting mate availability) on male mate choosiness. We investigated amplexus establishment after separating mating pairs and presenting focal males with a novel, size-matched female from the same population. Our analysis revealed considerable effects of sex ratio and (to a lesser extent) population density on time until amplexus establishment (choosiness). Male amphipods are able to perceive variable social conditions (e.g., sex ratio) and modify their mating strategy accordingly: We found choosiness to be reduced in increasingly male-biased populations, whereas selectivity increases when sex ratio becomes female biased. With this, our study expands our limited knowledge on natural variations in male mate choosiness and illustrates the importance of sex ratio (i.e., level of competition) for male mating decisions in natural environments. Accounting for variation in sex ratios, therefore, allows envisioning a distinctive variation of choosiness in natural populations and highlights the importance of considering social background information in future behavioral studies.
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Studies on primate sense of smell are scarce, even though odours represent the main communicative channel for many nocturnal primates such as gray slender lorises (Loris lydekkerianus). Here, we investigate the influence of natural odours on communicative and social behaviours on a group of slender lorises housed at the Frankfurt Zoo. Previously collected chemical marks from unknown conspecifics, urine from a natural predator (rusty-spotted cats) and a control setup were introduced in random order to the group enclosure. We recorded chemical communication behaviours, such as marking and sniffing, social behaviours and general activities. Using generalized linear mixed-effect models, we found that the odours did not have an effect on marking, but on sniffing behaviours of the animals. Conspecific odours decreased the sniffing frequencies of the animals (especially shortly after introduction). When predator odours were introduced, sniffing increased when compared to treatments with conspecific odours, but not in comparison to control treatments. The frequency of social behaviours, feeding and self-grooming did not change in response to predator or conspecific odours. Despite some limitations to our study, the data show a trend that natural odours may trigger some interest in group-kept slender lorises, and further examination of other novel odours may be worth studying (e.g. for potential chemical enrichment in zoos).
Asunto(s)
Lorisidae , Animales , Aseo Animal , Lorisidae/fisiología , Olfato , Conducta SocialRESUMEN
BACKGROUND: Efficient transfer of chemical signals is important for successful mating in many animal species. Multiple evolutionary lineages of animals evolved direct sex pheromone transmission during traumatic mating-the wounding of the partner with specialized devices-which helps to avoid signal loss to the environment. Although such direct transmission modes of so-called allohormone pheromones are well-documented in invertebrates, they are considered rare in vertebrates. Males of several species of the frog genus Plectrohyla (Hylidae, Anura) have elongated teeth and develop swollen lips during the breeding season. Here we investigated the possibility that these structures are used to scratch the females' skin and apply allohormone pheromones during traumatic mating in several Plectrohyla species. RESULTS: Our behavioural observations revealed that males press their upper jaw onto the females' dorsum during amplexus, leaving small skin scratches with their teeth. Histological examinations of the males' lips identified specialized mucus glands, resembling known amphibian pheromone glands. Whole-transcriptome sequencing of these breeding glands showed high expression of sodefrin precursor-like factor (SPF) proteins, which are known to have a pheromone function in multiple amphibian species. CONCLUSIONS: Our study suggests SPF delivery via traumatic mating in several anuran species: the males have specialized breeding glands in the lips for production and secretion and use their elongated teeth as wounding devices for application. We hypothesize that these SPF proteins end up in the females' circulatory system, where understanding their exact function will require further molecular, physiological and behavioural testing.
RESUMEN
Despite rising interest among scientists for over two centuries, parental care behavior has not been as thoroughly studied in amphibians as it has in other taxa. The first reports of amphibian parental care date from the early 18th century, when Maria Sibylla Merian went on a field expedition in Suriname and reported frog metamorphs emerging from their mother's dorsal skin. Reports of this and other parental behaviors in amphibians remained descriptive for decades, often as side notes during expeditions with another purpose. However, since the 1980s, experimental approaches have proliferated, providing detailed knowledge about the adaptive value of observed behaviors. Today, we recognize more than 30 types of parental care in amphibians, but most studies focus on just a few families and have favored anurans over urodeles and caecilians. Here, we provide a synthesis of the last three centuries of parental care research in the three orders comprising the amphibians. We draw attention to the progress from the very first descriptions to the most recent experimental studies, and highlight the importance of natural history observations as a source of new hypotheses and necessary context to interpret experimental findings. We encourage amphibian parental care researchers to diversify their study systems to allow for a more comprehensive perspective of the behaviors that amphibians exhibit. Finally, we uncover knowledge gaps and suggest new avenues of research using a variety of disciplines and approaches that will allow us to better understand the function and evolution of parental care behaviors in this diverse group of animals.
RESUMEN
Chemical signaling in animals often plays a central role in eliciting a variety of responses during reproductive interactions between males and females. One of the best-known vertebrate courtship pheromone systems is sodefrin precursor-like factors (SPFs), a family of two-domain three-finger proteins with a female-receptivity enhancing function, currently only known from salamanders. The oldest divergence between active components in a single salamander species dates back to the Late Paleozoic, indicating that these proteins potentially gained a pheromone function earlier in amphibian evolution. Here, we combined whole transcriptome sequencing, proteomics, histology, and molecular phylogenetics in a comparative approach to investigate SPF occurrence in male breeding glands across the evolutionary tree of anurans (frogs and toads). Our study shows that multiple families of both terrestrially and aquatically reproducing frogs have substantially increased expression levels of SPFs in male breeding glands. This suggests that multiple anuran lineages make use of SPFs to complement acoustic and visual sexual signaling during courtship. Comparative analyses show that anurans independently recruited these proteins each time the gland location on the male's body allowed efficient transmission of the secretion to the female's nares.
Asunto(s)
Anuros/metabolismo , Atractivos Sexuales/metabolismo , Animales , Anuros/genética , Glándulas Exocrinas/metabolismo , Femenino , Masculino , Oligopéptidos/metabolismo , Filogenia , Caracteres Sexuales , Secuenciación del ExomaRESUMEN
Although the involvement of peptide hormones in parental care behaviors is well investigated in vertebrates, in amphibians the physiological basis of parental care is largely unknown. This is all the more surprising as parental care behaviors in these tetrapods are remarkably diverse. The poison frog Ranitomeya imitator performs biparental care, including clutch guarding, tadpole transportation and nutrient provisioning. Here we tested whether the nonapeptides arginine-vasotocin (AVT) and mesotocin (MT) are involved in clutch guarding and tadpole transportation in these frogs. In ex-sito experiments we injected males and females after clutch deposition and before tadpole transport with AVT and MT, respectively, as well as their antagonist or a control. We measured two types of egg caring behavior (intense and general care) and compared the success rate of tadpole transportation after treatments. Surprisingly we found that AVT did not trigger, but decreased intense egg care behaviors in males and females. However, there was a trend for general care behavior to increase, which might explain the adverse effect regarding intense care. MT did not have an effect on egg caring behaviors, but after administration of this hormone males were less likely to transport their offspring later on. Our results indicate that AVT might be partly involved in egg caring behaviors in R. imitator, while MT does not appear to play any role in behaviors prior to tadpole transportation in males. This implies that other hormones, such as steroids or prolactin are likely to be important for early parental care behaviors in poison frogs.
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Anuros/fisiología , Conducta Materna/efectos de los fármacos , Oxitócicos/farmacología , Oxitocina/análogos & derivados , Conducta Paterna/efectos de los fármacos , Vasotocina/farmacología , Animales , Femenino , Modelos Lineales , Masculino , Oxitocina/farmacología , Estadísticas no ParamétricasRESUMEN
Stynoski et al. introduce the dendrobatids, a charismatic group of frogs known for their colourful and often poisonous skin.
Asunto(s)
Anuros/fisiología , Venenos/metabolismo , Animales , Anuros/metabolismo , Femenino , Masculino , Piel/metabolismo , Pigmentación de la Piel , Toxinas Biológicas/metabolismoRESUMEN
The evolution of chemical communication and the discrimination between evolved functions (signals) and unintentional releases (cues) are among the most challenging issues in chemical ecology. The accurate classification of inter- or intraspecific chemical communication is often puzzling. Here we report on two different communication systems triggering the same parental care behavior in the poison frog Ranitomeya variabilis. This species deposits its tadpoles and egg clutches in phytotelmata and chemically recognizes and avoids sites with both predatory conspecific and non-predatory heterospecific tadpoles (of the species Hyloxalus azureiventris). Combining chemical analyses with in-situ bioassays, we identified the molecular formulas of the chemical compounds triggering this behavior. We found that both species produce distinct chemical compound combinations, suggesting two separate communication systems. Bringing these results into an ecological context, we classify the conspecific R. variabilis compounds as chemical cues, advantageous only to the receivers (the adult frogs), not the emitters (the tadpoles). The heterospecific compounds, however, are suggested to be chemical signals (or cues evolving into signals), being advantageous to the emitters (the heterospecific tadpoles) and likely also to the receivers (the adult frogs). Due to these assumed receiver benefits, the heterospecific compounds are possibly synomones which are advantageous to both emitter and receiver â a very rare communication system between animal species, especially vertebrates.
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Comunicación Animal , Anuros/fisiología , Señales (Psicología) , Percepción Olfatoria , Feromonas , Conducta Predatoria , Animales , Anuros/genética , Comportamiento de Nidificación , Olfato , SimpatríaRESUMEN
The protection of offspring against predators and competitors is especially important in organisms using spatially separated breeding resources, impeding the offspring's chances to escape. One example of such isolated reproductive resources are phytotelmata (small water bodies in plant axils), exploited by the Neotropical poison frog Ranitomeya variabilis (Dendrobatidae) for both clutch and tadpole deposition. Because poison frog tadpoles are often cannibalistic, parents tend to avoid deposition with conspecifics. Previous studies have shown that this avoidance is based on chemical cues produced by conspecific tadpoles. Further, cues produced by phylogenetically less-related tadpoles (Bufonidae) were avoided for clutch but not tadpole depositions. We analyzed how the different responses to tadpole cues are triggered. We tested the reactions of parental R. variabilis to tadpole cues of species differing in two aspects: whether or not they are dendrobatids, and whether or not they reproduce in phytotelmata. We found that for clutch deposition, tadpole cues were always avoided, i.e., all tadpoles were treated by the frogs as if they pose a danger to the eggs. However, responses varied for tadpole depositions: while dendrobatid larvae living in phytotelmata were avoided, those breeding in streams were not. Non-poison frog tadpoles were ignored when associated with habitat other than phytotelmata, but they were preferred when living in phytotelmata. This suggests that both phylogeny and tadpole habitat are important triggers for the decisions made by R. variabilis. Only tadpoles using the same breeding resources are considered as relevant for the frog's own larvae (i.e., as a potential danger or food resource), while further decisions are related to evolutionary relationship.
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Bufonidae , Ranidae , Reproducción , Animales , Bufonidae/fisiología , Señales (Psicología) , Ecosistema , Femenino , Cadena Alimentaria , Humanos , Larva/fisiología , Masculino , Ranidae/fisiología , Reproducción/fisiologíaRESUMEN
Although anuran communication primarily takes place acoustically, chemical cues are also often used for intra- and intersexual communication in frogs. In the present study we analyzed the behavior of the poison frog Ranitomeya variabilis when presented chemical cues of same-sex or opposite-sex conspecifics. Chemical cues were obtained by keeping a single frog on a moist paper towel for about 47h. Afterwards two paper towels were offered to a test animal, one containing the chemical cues, the other containing rainwater only. We ran trials presenting female cues to males, males cues to males as well as male cues to females. The results of the trials were not significant in terms of intersexual communication. The overall response revealed a clear avoidance strategy which leads us to the assumption that disturbance cues unintentionally occurred during the experiment. The rather small size of the containers used to obtain chemical cues prior to the trials probably lead to confinement stress which consequently caused increased urination containing stress hormones that were detected by the test animals. This is the first proof of disturbance cues and their effects in adult anurans. The results of this study do not allow conclusions about inter- or intrasexual chemical communication of R. variabilis, but they allow implications and revisions for future experiments on this topic.