Genomic Signature of Shifts in Selection in a Subalpine Ant and Its Physiological Adaptations.

Understanding how organisms adapt to extreme environments is fundamental and can provide insightful case studies for both evolutionary biology and climate-change biology. Here, we take advantage of the vast diversity of lifestyles in ants to identify genomic signatures of adaptation to extreme habitats such as high altitude. We hypothesized two parallel patterns would occur in a genome adapting to an extreme habitat: 1) strong positive selection on genes related to adaptation and 2) a relaxation of previous purifying selection. We tested this hypothesis by sequencing the high-elevation specialist Tetramorium alpestre and four other phylogenetically related species. In support of our hypothesis, we recorded a strong shift of selective forces in T. alpestre, in particular a stronger magnitude of diversifying and relaxed selection when compared with all other ants. We further disentangled candidate molecular adaptations in both gene expression and protein-coding sequence that were identified by our genome-wide analyses. In particular, we demonstrate that T. alpestre has 1) a higher level of expression for stv and other heat-shock proteins in chill-shock tests and 2) enzymatic enhancement of Hex-T1, a rate-limiting regulatory enzyme that controls the entry of glucose into the glycolytic pathway. Together, our analyses highlight the adaptive molecular changes that support colonization of high-altitude environments.

Evolutionary history of inquiline social parasitism in Plagiolepis ants.

Social parasitism, i.e. the parasitic dependence of a social species on another free-living social species, is one of the most intriguing phenomena in social insects. It has evolved to various levels, the most extreme form being inquiline social parasites which have lost the worker caste, and produce only male and female sexual offspring that are reared by the host worker force. The inquiline syndrome has been reported in 4 species within the ant genus Plagiolepis, in Europe. Whether inquiline social parasitism evolved once or multiple times within the genus remains however unknown. To address this question, we generated data for 5 inquiline social parasites - 3 species previously described and 2 unidentified species - and their free-living hosts from Europe, and we inferred their phylogenetic relationships. We tested Emery's rule, which predicts that inquiline social parasites and their hosts are close relatives. Our results show that inquiline parasitism evolved independently at least 5 times in the genus. Furthermore, we found that all inquilines were associated with one of the descendants of their most related free-living species, suggesting sympatric speciation is the main process leading to the emergence of the parasitic species, consistent with the stricter version of Emery's rule.

Evolution of morphological crypsis in the Tetramorium caespitum ant species complex (Hymenoptera: Formicidae).

Cryptic species are morphologically very similar to each other. To what extent stasis or convergence causes crypsis and whether ecology influences the evolution of crypsis has remained unclear. The Tetramorium caespitum complex is one of the most intricate examples of cryptic species in ants. Here, we test three hypotheses concerning the evolution of its crypsis: H1: The complex is monophyletic. H2: Morphology resulted from evolutionary stasis. H3: Ecology and morphology evolved concertedly. We confirmed (H1) monophyly of the complex; (H2) a positive relation between morphological and phylogenetic distances, which indicates a very slow loss of similarity over time and thus stasis; and (H3) a positive relation between only one morphological character and a proxy of the ecological niche, which indicates concerted evolution of these two characters, as well as a negative relation between p-values of correct species identification and altitude, which suggests that species occurring in higher altitudes are more cryptic. Our data suggest that species-specific morphological adaptations to the ecological niche are exceptions in the complex, and we consider the worker morphology in this complex as an adaptive solution for various environments.

A near-infrared spectroscopy routine for unambiguous identification of cryptic ant species.

Species identification-of importance for most biological disciplines-is not always straightforward as cryptic species hamper traditional identification. Fibre-optic near-infrared spectroscopy (NIRS) is a rapid and inexpensive method of use in various applications, including the identification of species. Despite its efficiency, NIRS has never been tested on a group of more than two cryptic species, and a working routine is still missing. Hence, we tested if the four morphologically highly similar, but genetically distinct ant species Tetramorium alpestre, T. caespitum, T. impurum, and T. sp. B, all four co-occurring above 1,300 m above sea level in the Alps, can be identified unambiguously using NIRS. Furthermore, we evaluated which of our implementations of the three analysis approaches, partial least squares regression (PLS), artificial neural networks (ANN), and random forests (RF), is most efficient in species identification with our data set. We opted for a 100% classification certainty, i.e., a residual risk of misidentification of zero within the available data, at the cost of excluding specimens from identification. Additionally, we examined which strategy among our implementations, one-vs-all, i.e., one species compared with the pooled set of the remaining species, or binary-decision strategies, worked best with our data to reduce a multi-class system to a two-class system, as is necessary for PLS. Our NIRS identification routine, based on a 100% identification certainty, was successful with up to 66.7% of unambiguously identified specimens of a species. In detail, PLS scored best over all species (36.7% of specimens), while RF was much less effective (10.0%) and ANN failed completely (0.0%) with our data and our implementations of the analyses. Moreover, we showed that the one-vs-all strategy is the only acceptable option to reduce multi-class systems because of a minimum expenditure of time. We emphasise our classification routine using fibre-optic NIRS in combination with PLS and the one-vs-all strategy as a highly efficient pre-screening identification method for cryptic ant species and possibly beyond.

Genomic Resources Notes accepted 1 February 2015 - 31 March 2015.

This article documents the public availability of (i) raw transcriptome sequence data, assembled contigs and BLAST hits of the Antarctic plant Colobanthus quitensis grown in two different climatic conditions, (ii) the draft genome sequence data (raw reads, assembled contigs and unassembled reads) and RAD-tag read data of the marbled flounder Pseudopleuronectes yokohamae, (iii) transcriptome resources from four white campion (Silene latifolia) individuals from two morphologically divergent populations and (iv) nuclear DNA markers from 454 sequencing of reduced representation libraries (RRL) based on amplified fragment length polymorphism (AFLP) PCR products of four species of ants in the genus Tetramorium.