Selection can facilitate diversification by inducing character displacement in mate choice traits that reduce the probability of maladaptive mating between lineages. Although reproductive character displacement (RCD) has been demonstrated in two-taxa case studies, the frequency of this process in nature is still debated. Moreover, studies have focused primarily on visual and acoustic traits, despite the fact that chemical communication is probably the most common means of species recognition. Here, we showed in a large, mostly sympatric, butterfly genus, a strong pattern of recurrent RCD for predicted male sex pheromone composition, but not for visual mate choice traits. Our results suggest that RCD is not anecdotal, and that selection for divergence in male sex pheromone composition contributed to reproductive isolation within the Bicyclus genus. We propose that selection may target olfactory mate choice traits as a more common sensory modality to ensure reproductive isolation among diverging lineages than previously envisaged.
Mitochondrial markers are still often used alone to identify evolutionary units, despite widespread evidence for processes such as incomplete lineage sorting or introgressive hybridization that may blur past population history. The combination of mitochondrial DNA data with other sources of information (morphology, nuclear genes) is a powerful tool to reveal when and why mitochondrial markers are potentially misleading. In this study, we evaluate the performance of mtDNA markers to unravel the evolutionary history of Spanish lizards from the Podarcis hispanicus species complex. We first uncover several cases of discordance between morphological and mitochondrial data in delimitation of taxa. To assess the origin of these discordances, we analysed the same populations using several independent nuclear loci. Both morphological and nuclear markers identified the same three evolutionary units in the region, while mitochondrial data revealed four deeply divergent lineages. We suggest here that the most likely scenario to explain this discordance is ancient mitochondrial introgression originating from a fourth evolutionary unit presently absent from the study area. Notably, this resulted in a complete replacement of the original lineage in a large part of the distribution of one of the taxa investigated. We discuss the potential evolutionary scenarios leading to this complete mitochondrial replacement and suggest why the previous studies have failed to recover the correct history of this species complex.
Chemical communication in insects' sexual interactions is well-known to involve olfaction of volatile compounds called sex pheromones. In theory, sexual chemical communication may also involve chemicals with low or no volatility exchanged during precopulatory gustatory contacts. Yet, knowledge on this latter type of chemicals is so far mostly restricted to the Drosophila fly model. Here we provide the most comprehensive characterization to date of the cuticular chemical profile, including both volatile and non-volatile compounds, of a model butterfly, Bicyclus anynana. First, we characterized the body distribution of 103 cuticular lipids, mostly alkanes and methyl-branched alkanes, by gas chromatography coupled to mass spectrometry (GC-MS). Second, we developed a multivariate statistical approach to cope with such complex chemical profiles and showed that variation in the presence or abundance of a subset of the cuticular lipids indicated body parts, and traits involved in B. anynana mate choice, namely sex and age. Third, we identified the chemical structure of the 20 most indicative compounds, which were on average more abundant (1346.4 ± 1994.6 ng; mean ± SD) than other, likely less indicative, compounds (225.9 ± 507.2 ng; mean ± SD). Fourth, we showed that wings and legs displayed most of the chemical information found on the entire body of the butterflies. Fifth, we showed that non-random gustatory contacts occurred between specific male and female body parts during courtship. The body parts mostly touched by the conspecific displayed the largest between-sex differentiation in cuticular composition. Altogether, the large diversity of cuticular lipids in B. anynana, which exceeds the one of Drosophila flies, and its non-random distribution and evaluation across individuals, together suggest that gustatory information is likely exchanged during sexual interactions in Lepidoptera.
Sexual traits are often the most divergent characters among closely related species, suggesting an important role of sexual traits in speciation. However, to prove this, we need to show that sexual trait differences accumulate before or during the speciation process, rather than being a consequence of it. Here, we contrast patterns of divergence among putative male sex pheromone (pMSP) composition and the genetic structure inferred from variation in the mitochondrial cytochrome oxidase 1 and nuclear CAD loci in the African butterfly Bicyclus anynana (Butler, 1879) to determine whether the evolution of “pheromonal dialects” occurs before or after the differentiation process. We observed differences in abundance of some shared pMSP components as well as differences in the composition of the pMSP among B. anynana populations. In addition, B. anynana individuals from Kenya displayed differences in the pMSP composition within a single population that appeared not associated with genetic differences. These differences in pMSP composition both between and within B. anynana populations were as large as those found between different Bicyclus species. Our results suggest that “pheromonal dialects” evolved within and among populations of B. anynana and may therefore act as precursors of an ongoing speciation process.
Recent genetic works have suggested that the Iberian wall lizard Podarcis hispanicus (Steindachner, 1870) sensu lato is in fact a species complex. Several forms have already been elevated to species rank, including the north-eastern Spanish form alternatively named Podarcis atratus (Boscá, 1916) or P. liolepis (Boulenger, 1905) in different works. However, a recent study has demonstrated that the province of Valencia, where most individuals of the type series of Lacerta muralis var. liolepis Boulenger, 1905 originate from, is inhabited by populations that are conspecific with the north-eastern Spanish form. Consequently the nomen liolepis has precedence over atratus to designate the north-eastern species of the P. hispanicus complex which should thus bear the name Podarcis liolepis.
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