Social Parasite Ants in the Alps: a New Site of the Vulnerable Myrmica myrmicoxena and New Uppermost Altitudinal Limit for M. microrubra

We conducted a survey on the Alpine fauna of one of the largest Natural Park of the Italian Alps (Stelvio National Park) in the framework of a broad ecological monitoring of Alpine biodiversity. A two-years standardized sampling employing pitfall traps along a 1200 m altitudinal gradient led to the discovery of two interesting inquiline social parasite ants of the genus Myrmica: M. myrmicoxena Forel, 1895 and M. microrubra Seifert, 1993. Myrmica myrmicoxena, which is classified as Vulnerable according to the IUCN Red List, was so far known from only three sites across a narrow geographic range between Italy and Switzerland. Our data support the previous hypothesis over its ecology and host association. Myrmica microrubra is considered an incipient species of high evolutionary interest, sometimes regarded as an intraspecific form of M. rubra. While having a wide distribution in Europe, its presence in Italy was hitherto known only from a single site, and our record extends its altitudinal distribution limit in Europe upwards by about 600 m.

A new ant-butterfly symbiosis in the forest canopy fills an evolutionary gap

Myrmecophilous butterflies can establish complex symbiotic relationships with ants. A caterpillar wandering among the brood of the aggressive ponerine ant Neoponera villosa was found inside the core of a nest built in the myrmecophytic bromeliad Aechmea bracteata. This is the first caterpillar found living inside a ponerine ant nest. Its DNA barcode was sequenced, and an integrative approach was used to identify it as Pseudonymphidia agave, a poorly known member of the subtribe Pachythonina in the riodinid tribe Nymphidiini. The cuticle of the tank-like caterpillar lacks projections or tubercles and is covered dorsally by specialized flat setae that form an armor of small plates. Ant-organs potentially related to caterpillar-ant signaling, such as perforated cupola organs and tentacle nectary organs, are present. These morphological traits, together with evidence of social integration (direct contact with host brood, protective morphology, slow movement, no host aggressiveness), suggest that P. agave is a symbiotic, social parasite of N. villosa, preying on its host brood. However, several knowledge gaps remain, including oviposition site, dependence on bromeliad association, steps to colony integration, and larval diet through development. Carnivory has been reported in all known members of the subtribe Pachythonina (caterpillars prey on honeydew-producing hemipterans) suggesting a shift to myrmecophagy inside the ant nests as a possible evolutionary transition.

Karyotype structure and cytogenetic markers of Amoimyrmex bruchi and Amoimyrmex silvestrii: the contribution to understanding leafcutting ant relationships

Leafcutting ants are considered the most important herbivores in terrestrial environments throughout the Neotropics. <i>Amoimyrmex</i> is the sister clade of the remaining leafcutter ants from the genera <i>Atta</i> and <i>Acromyrmex</i>. <i>Amoimyrmex striatus</i> was the only species cytogenetically studied within the genus and shares the same chromosomal number with <i>Atta</i>, bearing 22 chromosomes, whereas <i>Acromyrmex</i> bears 38 chromosomes, with the exception of the social parasite <i>Acromyrmex ameliae</i> (2n=36). Our objective here was to analyze cytogenetically the species of <i>Amoimyrmex bruchi</i> and <i>Amoimyrmex silvestrii</i>, as well as to describe the karyotype of these sister species, by means of an integrative approach using classical and molecular cytogenetics. We aimed to characterize cytogenetic markers that contribute to the systematics and taxonomy of the genus. Our results showed that the karyotypes of these two species are very similar, with an identical chromosome number (2n=22), chromosome morphology (2K=20m+2sm), and location of 18S rDNA and the telomeric repeat TTAGG on the chromosomes. Yet, the microsatellite probe GA(15) showed variation across the species and populations studied. We suggest that both species diverged relatively recently and are unmistakably sisters because of the many shared characteristics, including the highly conserved karyotypes.

Filling the gap: a new ant-butterfly symbiosis in the forest canopy

Myrmecophilous butterflies can establish complex symbiotic relationships with ants. An elusive symbiotic caterpillar wandering among the brood of the aggressive ponerine ant, Neoponera villosa, was found inside the core of a nest built in the myrmecophytic bromeliad Aechmea bracteata. This is the first caterpillar found in symbiosis with a species of the subfamily Ponerinae. Tissue sample was barcoded, and an integrative approach was used to identify it as Pseudonymphidia agave, a poorly known Pachythonina member in the riodinid myrmecophilous tribe Nymphidiini. The caterpillar has a general tank-like body morphology, without projections or tubercles, and is covered dorsally by specialized flat setae that form an armor of small plates. Ant-organs potentially related to the caterpillar-ant signaling, such as perforated cupola organs and tentacle nectary organs, are present. These functional traits, together with the stable social integration, suggest that P. agave is a specialized social parasite of N. villosa. However, several knowledge gaps remain, notably the oviposition site, dependence on bromeliad association, steps to colony integration, and the larval diet through ontogeny. Carnivory has been reported in all known members of the Pachythonina subtribe (caterpillars prey on honeydew-producing hemipterans), and a shift to myrmecophagy inside the ant nests is a possible evolutionary step.

Does effective population size affect rates of molecular evolution: mitochondrial data for host/parasite species pairs in bees suggests not

Adaptive evolutionary theory argues that organisms with larger effective population size (Ne) should have higher rates of adaptive evolution and therefore greater capacity to win evolutionary arm races. However, in some certain cases species with much smaller Ne may be able to survive beside their opponents for an extensive evolutionary time. Neutral theory predicts that accelerated rates of molecular evolution in organisms with exceedingly small Ne is due to the effects of genetic drift and fixation of slightly deleterious mutations. We test this prediction in two obligate social parasite species and their respective host species from the bee tribe Allodapini. The parasites (genus Inquilina) have been locked into a tight coevolutionary arm races with their exclusive hosts (genus Exoneura) for ~15 million years, even though Inquilina exhibit Ne that are an order of magnitude smaller than their host. In this study, we compared rates of molecular evolution between host and parasite using nonsynonymous to synonymous substitution rate ratios (dN/dS) of eleven mitochondrial protein coding genes sequenced from transcriptomes. Tests of selection on mitochondrial genes indicated no significant differences between host and parasite dN/dS, with evidence for purifying selection acting on all mitochondrial genes of host and parasite species. Several potential factors which could weaken the inverse relationship between Ne and rate of molecular evolution are discussed.

Queens of the inquiline social parasite Acromyrmex insinuator can join nest-founding queens of its host, the leaf-cutting ant Acromyrmex echinatior

Queens of the inquiline social parasite Acromyrmex insinuator are known to infiltrate mature colonies of Acromyrmex echinatior and to exploit the host’s perennial workforce by producing predominantly reproductive individuals while suppressing host reproduction. Here we report three cases of an A. insinuator queen having joined an incipient colony of A. echinatior that contained only the founding host-queen and her small symbiotic fungus garden. We conjectured that 1:1 host-inquiline co-founding—a phenomenon that has only rarely been reported in ants—may imply that the presence of an A. insinuator queen may incur benefits to the host by increasing survival of its incipient colonies. We observed that the parasite queens neither foraged nor defended the nest against intruders. However, the parasite queens interacted with the host and fungus in a way that could be consistent with grooming and/or with contributing eggs. These observations may help explain why A. insinuator queens have maintained metapleural glands, even though they are smaller than those of host queens, and why A. insinuator has lost the large foraging worker caste but not the small worker caste.

First observation of an ant colony of Formica fuscocinerea Forel, 1874 invaded by the social parasite F. truncorum Fabricius, 1804 (Hymenoptera, Formicidae)

In the northern Alps of Switzerland we observed a mixed ant colony of Formica truncorum Fabricius, 1804 and F. fuscocinerea Forel, 1874 at the foot of a schoolhouse wall in the built-up centre of the small town of Näfels (canton of Glarus). Based on the fact that the habitat is favorable only for F. fuscocinerea and that F. truncorum is a notorious temporary social parasite, we conclude that in this case a colony of F. fuscocinerea must have been usurped by F. truncorum. This is remarkable, as it is the first reported case where a colony of F. fuscocinerea has been taken over by a social parasite. We consider the observed unusually small workers of F. truncorum to be a starvation form. This is probably due to the suboptimal urban nest site, as this species typically occurs along the edge of forests or in clearings.

Relaxed selection underlies genome erosion in socially parasitic ant species

Inquiline ants are highly specialized and obligate social parasites that infiltrate and exploit colonies of closely related species. They have evolved many times convergently, are often evolutionarily young lineages, and are almost invariably rare. Focusing on the leaf-cutting ant genus Acromyrmex, we compared genomes of three inquiline social parasites with their free-living, closely-related hosts. The social parasite genomes show distinct signatures of erosion compared to the host lineages, as a consequence of relaxed selective constraints on traits associated with cooperative ant colony life and of inquilines having very small effective population sizes. We find parallel gene losses, particularly in olfactory receptors, consistent with inquiline species having highly reduced social behavioral repertoires. Many of the genomic changes that we uncover resemble those observed in the genomes of obligate non-social parasites and intracellular endosymbionts that branched off into highly specialized, host-dependent niches.