Mutualistic interaction of aphids and ants in pepper, Capsicum annuum and Capsicum frutenscens (Solanaceae) / Interacción mutualista de pulgones y hormigas en pimiento, Capsicum annuum y Capsicum frutenscens (Solanaceae)

Abstract Introduction: Adequate biological identification is fundamental for establishing integrated pest management programs and identifying the trophic and mutualist relationships that can affect pest population dynamics. Aphids are the main pest of pepper Capsicum spp. (Solanaceae) crops in Southwestern Colombia, due to their role as vectors of viruses. However, the identification of aphid species is complex, limiting the investigations performed to address their interactions with other organisms. Ants and aphids present a facultative mutualistic relationship, that promotes the growth of hemipteran colonies, for this reason, the study of the ecological mutualistic association between aphids and ants is important. Objective: The main objective was to discriminate the aphid species present in commercial crops of Capsicum spp., and to identify the ant community that attends the aphid colonies and its effects on the size of the aphid colonies. Methods: Aphid species, and their ant mutualist, were collected from Capsicum annuum and Capsicum frutescens, in the Cauca valley, Southwestern Colombia. We used the DNA barcoding approach to identify aphid species, and the ants were identified by morphology-based taxonomy. To evaluate the effect of ant care on the size and structure of aphid colonies, generalized linear models were calculated using as the response variables the total number of aphids for each colony and the proportion of nymphs. Results: The aphid species that attack pepper crops, are: Aphis gossypii and Myzus persicae (Hemiptera: Aphididae), with A. gossypii being the species that interacts with ants (19 ant species). A. gossypii colonies attended by ants had larger sizes and more nymphs per colony, than those not attended. Conclusions: Although the aphid-ant interaction is not species-specific, it is necessary to consider its role in the propagation of viral diseases in peppers and to determine how this interaction may affect regional biological control strategies.

Resumen Introducción: La adecuada identificación biológica es fundamental para establecer programas de manejo integrado de plagas e identificar las relaciones tróficas y mutualistas que pueden afectar la dinámica poblacional de insectos plaga. Los áfidos son las principales plagas del ají Capsicum spp. (Solanaceae) en el suroccidente colombiano, debido a su rol como vectores de virus. Sin embargo, su identificación es compleja, y limita las investigaciones que intentan revelar sus interacciones con otros organismos. Las hormigas y los áfidos presentan una relación mutualista facultativa, que promueve el crecimiento de las colonias de los hemípteros, por esta razón, el estudio de la asociación ecológica y mutualista entre áfidos y hormigas es importante. Objetivo: El principal objetivo de esta investigación fue discriminar las especies de áfidos presentes en cultivos comerciales de Capsicum spp., e identificar la comunidad de hormigas que atiende las colonias de áfidos y su efecto en el tamaño de las colonias de áfidos. Métodos: Los áfidos, y las hormigas mutualistas de estos áfidos, se recolectaron de Capsicum annuum y Capsicum frutescens, en el valle del rio Cauca, en el suroccidente colombiano. Se empleó el Código de barras del ADN para identificar las especies de áfidos, y las hormigas se identificaron empleando taxonomía basada en morfología. Para evaluar el efecto que tiene el cuidado de las hormigas sobre el tamaño de las colonias de áfidos, se empleó un modelo lineal generalizado, utilizando como variables de respuesta el número total de áfidos por cada colonia y la proporción de ninfas por colonia. Resultados: Las especies de áfidos que atacan los cultivos de ají, son: Aphis gossypii y Myzus persicae (Hemiptera: Aphididae), siendo A. gossypii la especie que interactúa con hormigas (19 especies). Las colonias de A. gossypii atendidas por hormigas presentan mayor tamaño y número de ninfas, que aquellas desatendidas. Conclusiones: Aunque la interacción áfido-hormiga no es especie específica, es necesario considerar su rol en la propagación de enfermedades virales en plantas cultivadas y determinar cómo esta interacción puede afectar la implementación de estrategias de control biológico.

Skin transcriptional profiles in Oophaga poison frogs.

Aposematic organisms advertise their defensive toxins to predators using a variety of warning signals, including bright coloration. While most Neotropical poison frogs (Dendrobatidae) rely on crypsis to avoid predators, Oophaga poison frogs from South America advertise their chemical defenses, a complex mix of diet-derived alkaloids, by using conspicuous hues. The present study aimed to characterize the skin transcriptomic profiles of South American Oophaga poison frogs. Our analyses showed very similar transcriptomic profiles for these closely related species in terms of functional annotation and relative abundance of gene ontology terms expressed. Analyses of expression profiles of Oophaga and available skin transcriptomes of cryptic anurans allowed us to propose initial hypotheses for the active sequestration of alkaloid-based chemical defenses and to highlight some genes that may be potentially involved in resistance mechanisms to avoid self-intoxication and skin coloration. In doing so, we provide an important molecular resource for the study of warning signals that will facilitate the assembly and annotation of future poison frog genomes.

Complex patterns of differentiation and gene flow underly the divergence of aposematic phenotypes in Oophaga poison frogs.

Hybridization and introgression can have complex consequences for both species evolution and conservation. Here, we investigated the origin and characteristics of a putative hybrid zone between two South American poison dart frog species, Oophaga anchicayensis and the critically endangered Oophaga lehmanni, which are heavily sought after on the illegal pet market. Using a combination of phenotypic (49 traits) and genomic (ddRADseq) data, we found that the putative hybrids are morphologically distinct from their parental species and confirmed genomic signatures of admixture in these populations. Several lines of evidence (hybrid indices, interspecific hybrid heterozygosity, genomic clines, comparisons with simulated hybrids and demographic modelling) support the conclusion that these populations are not comprised of early-generation hybrids and thus, they probably did not arise as a result of illegal translocations associated with wildlife trafficking. Instead, they probably represent an independent lineage which has persisted through isolation and has only relatively recently re-established gene flow with both parental species. Furthermore, we detected signals of differential introgression from parental species into these hybrid populations which suggest relaxed stabilizing selection on these aposematic colour morphs, potentially via context-dependent female choice. These populations thus provide a fascinating window into the role of hybridization, isolation and female choice in the diversification of South American poison dart frogs. In addition, our results underline the importance of landscape conservation measures to protect, not only known localities of nominal species, but also the phenotypic and genomic variation harbored by admixed lineages which represent crucial repositories for the impressive diversity in this system.

Multivariate species boundaries and conservation of harlequin poison frogs.

In this study, we present an iterative method for delimiting species under the general lineage concept (GLC) based on the multivariate clustering of morphological, ecological and genetic data. Our rationale is that distinct multivariate groups correspond to evolutionarily independent metapopulation lineages because they reflect the common signal of different secondary defining properties (environmental and genetic distinctiveness, phenotypic diagnosability, etc.) that imply the existence of barriers preventing or limiting gene exchange. We applied this method to study a group of endangered poison frogs, the Oophaga histrionica complex. In our study case, we used next-generation targeted amplicon sequencing to obtain a robust genetic data set that we combined with patterns of morphological and ecological features. Our analyses revealed the existence of at least five different species in the histrionica complex (three, new to science), some of them, occurring in small isolated populations outside any protected areas. The lineage delimitation proposed here has important conservation implications as it revealed that some of the Oophaga species should be considered among the most vulnerable of the Neotropical frogs. More broadly, our study exemplifies how multiple-amplicon and multivariate statistical techniques can be integrated to successfully identify species and their boundaries.

Diversification and convergence of aposematic phenotypes: truncated receptors and cellular arrangements mediate rapid evolution of coloration in harlequin poison frogs.

Aposematic signals represent one of the classical systems to study evolution and, as such, they have received considerable empirical and theoretical investigation. Despite the extensive literature on aposematic coloration, much uncertainty remains about genetic changes responsible for the repeated evolution of similar signals in multiple lineages. Here, we study the diversification and convergence of coloration among lineages of aposematic harlequin poison frogs (Oophaga histrionica complex). Our results suggest that different background phenotypes, showing different color and/or luminance contrast, have evolved independently at least twice in this group. We suggest that cellular arrangements are behind the striking diversity of color and patterns in this group and propose that differences in dorsal background color may be related to either or both, the presence/absence of xanthophores and the dispersion of melanosomes. Our genetic analyses support a role for the melanocortin receptor MC1R in melanosome aggregation, and we show evidence that two different mutations (∆433 and C432A) are responsible for the darker phenotypes that may display a more detectable, easier to learn, aposematic signal.