A Social Parasite Evolved Reproductive Isolation from Its Fungus-Growing Ant Host in Sympatry

SummaryInquiline social parasitic ant species exploit colonies of other ant species mainly by producing sexual offspring that are raised by the host. Ant social parasites and their hosts are often close relatives (Emery’s rule), and two main hypotheses compete to explain the parasites’ evolutionary origins: (1) the interspecific hypothesis proposes an allopatric speciation scenario for the parasite, whereas (2) the intraspecific hypothesis postulates that the parasite evolves directly from its host in sympatry [1–10]. Evidence in support of the intraspecific hypothesis has been accumulating for ants [3, 5, 7, 9–12], but sympatric speciation remains controversial as a general speciation mechanism for inquiline parasites. Here we use molecular phylogenetics to assess whether the socially parasitic fungus-growing ant Mycocepurus castrator speciated from its host Mycocepurus goeldii in sympatry. Based on differing patterns of relationship in mitochondrial and individual nuclear genes, we conclude that host and parasite occupy a temporal window in which lineage sorting has taken place in the mitochondrial genes but not yet in the nuclear alleles. We infer that the host originated first and that the parasite originated subsequently from a subset of the host species’ populations, providing empirical support for the hypothesis that inquiline parasites can evolve reproductive isolation while living sympatrically with their hosts

The rediscovery of the putative ant social parasite Manica parasitica syn. nov. (Hymenoptera: Formicidae) reveals an unexpected endoparasite syndrome

Parasitism is ubiquitous across the tree of life, and parasites comprise approximately half of all animal species. Social insect colonies attract many pathogens, endo- and ectoparasites, and are exploited by social parasites, which usurp the social environment of their hosts for survival and reproduction. Exploitation by parasites and pathogens versus social parasites may cause similar behavioural and morphological modifications of the host. Ants possess two overlapping syndromes: the endo- and social parasite syndromes. We rediscovered two populations of the putative social parasite Manica parasitica in the Sierra Nevada, and tested the hypothesis that M. parasitica is an independently evolving social parasite. We evaluated traits used to discriminate M. parasitica from its host Manica bradleyi, and examined the morphology of M. parasitica in the context of ant parasitic syndromes. We find that M. parasitica is not a social parasite. Instead, M. parasitica represents cestode-infected M. bradleyi. We propose that M. parasitica should be regarded as a junior synonym of M. bradleyi. Our results emphasize that an integrative approach is essential for unravelling the complex life histories of social insects and their symbionts

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

Reciprocal genomic evolution in the ant-fungus agricultural symbiosis

The attine ant–fungus agricultural symbiosis evolved over tens of millions of years, producing complex societies with industrial-scale farming analogous to that of humans. Here we document reciprocal shifts in the genomes and transcriptomes of seven fungus-farming ant species and their fungal cultivars. We show that ant subsistence farming probably originated in the early Tertiary (55–60 MYA), followed by further transitions to the farming of fully domesticated cultivars and leaf-cutting, both arising earlier than previously estimated. Evolutionary modifications in the ants include unprecedented rates of genome-wide structural rearrangement, early loss of arginine biosynthesis and positive selection on chitinase pathways. Modifications of fungal cultivars include loss of a key ligninase domain, changes in chitin synthesis and a reduction in carbohydrate-degrading enzymes as the ants gradually transitioned to functional herbivory. In contrast to human farming, increasing dependence on a single cultivar lineage appears to have been essential to the origin of industrial-scale ant agriculture

Molecular phylogeny of Indo‐Pacific carpenter ants (Hymenoptera: Formicidae, Camponotus) reveals waves of dispersal and colonization from diverse source areas

Ants that resemble Camponotus maculatus (Fabricius, 1782) present an opportunity to test the hypothesis that the origin of the Pacific island fauna was primarily New Guinea, the Philippines, and the Indo‐Malay archipelago (collectively known as Malesia). We sequenced two mitochondrial and four nuclear markers from 146 specimens from Pacific islands, Australia, and Malesia. We also added 211 specimens representing a larger worldwide sample and performed a series of phylogenetic analyses and ancestral area reconstructions. Results indicate that the Pacific members of this group comprise several robust clades that have distinctly different biogeographical histories, and they suggest an important role for Australia as a source of Pacific colonizations. Malesian areas were recovered mostly in derived positions, and one lineage appears to be Neotropical. Phylogenetic hypotheses indicate that the orange, pan‐Pacific form commonly identified as C. chloroticus Emery 1897 actually consists of two distantly related lineages. Also, the lineage on Hawaiʻi, which has been called C. variegatus (Smith, 1858), appears to be closely related to C. tortuganus Emery, 1895 in Florida and other lineages in the New World. In Micronesia and Polynesia the C. chloroticus‐like species support predictions of the taxon‐cycle hypothesis and could be candidates for human‐mediated dispersal.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/112260/1/cla12099-sup-0002-FigureS2.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/112260/2/cla12099-sup-0003-FigureS3.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/112260/3/cla12099-sup-0001-FigureS1.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/112260/4/cla12099-sup-0004-FigureS4.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/112260/5/cla12099-sup-0005-FigureS5.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/112260/6/cla12099-sup-0006-FigureS6.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/112260/7/cla12099.pd

An ant genus-group ( Prenolepis ) illuminates the biogeography and drivers of insect diversification in the Indo-Pacific

The Malay Archipelago and the tropical South Pacific (hereafter the Indo-Pacific region) are considered biodiversity hotspots, yet a general understanding of the origins and diversification of species-rich groups in the region remains elusive. We aimed to test hypotheses for the evolutionary processes driving insect species diversity in the Indo-Pacific using a higher-level and comprehensive phylogenetic hypothesis for an ant clade consisting of seven genera. We estimated divergence times and reconstructed the biogeographical history of ant species in the Prenolepis genus-group (Formicidae: Formicinae: Lasiini). We used a fossil-calibrated phylogeny to infer ancestral geographical ranges utilizing a biogeographic model that includes founder-event speciation. Ancestral state reconstructions of the ants\u27 ecological preferences, and diversification rates were estimated for selected Indo-Pacific clades. Overall, we report that faunal interchange between Asia and Australia has occurred since at least 20–25 Ma, and early dispersal to the Fijian Basin happened during the early and mid-Miocene (ca. 10–20 Ma). Differences in diversification rates across Indo-Pacific clades may be related to ecological preference breadth, which in turn may have facilitated geographical range expansions. Ancient dispersal routes suggested by our results agree with the palaeogeography of the region. For this particular group of ants, the rapid orogenesis in New Guinea and possibly subsequent ecological shifts may have promoted their rapid diversification and widespread distribution across the Indo-Pacific

Thelytokous Parthenogenesis in the Fungus-Gardening Ant Mycocepurus smithii (Hymenoptera: Formicidae)

The general prevalence of sexual reproduction over asexual reproduction among organisms testifies to the evolutionary benefits of recombination, such as accelerated adaptation to changing environments and elimination of deleterious mutations. Documented instances of asexual reproduction in groups otherwise dominated by sexual reproduction challenge evolutionary biologists to understand the special circumstances that might confer an advantage to asexual reproductive strategies. Here we report one such instance of asexual reproduction in the ants. We present evidence for obligate thelytoky in the asexual fungus-gardening ant, Mycocepurus smithii, in which queens produce female offspring from unfertilized eggs, workers are sterile, and males appear to be completely absent. Obligate thelytoky is implicated by reproductive physiology of queens, lack of males, absence of mating behavior, and natural history observations. An obligate thelytoky hypothesis is further supported by the absence of evidence indicating sexual reproduction or genetic recombination across the species' extensive distribution range (Mexico-Argentina). Potential conflicting evidence for sexual reproduction in this species derives from three Mycocepurus males reported in the literature, previously regarded as possible males of M. smithii. However, we show here that these specimens represent males of the congeneric species M. obsoletus, and not males of M. smithii. Mycocepurus smithii is unique among ants and among eusocial Hymenoptera, in that males seem to be completely absent and only queens (and not workers) produce diploid offspring via thelytoky. Because colonies consisting only of females can be propagated consecutively in the laboratory, M. smithii could be an adequate study organism a) to test hypotheses of the population-genetic advantages and disadvantages of asexual reproduction in a social organism and b) inform kin conflict theory

Biogeography of mutualistic fungi cultivated by leafcutter ants

Leafcutter ants propagate co-evolving fungi for food. The nearly 50 species of leafcutter ants (Atta, Acromyrmex) range from Argentina to the United States, with the greatest species diversity in southern South America. We elucidate the biogeography of fungi cultivated by leafcutter ants using DNA sequence and microsatellite-marker analyses of 474 cultivars collected across the leafcutter range. Fungal cultivars belong to two clades (Clade-A and Clade-B). The dominant and widespread Clade-A cultivars form three genotype clusters, with their relative prevalence corresponding to southern South America, northern South America, Central and North America. Admixture between Clade-A populations supports genetic exchange within a single species, Leucocoprinus gongylophorus. Some leafcutter species that cut grass as fungicultural substrate are specialized to cultivate Clade-B fungi, whereas leafcutters preferring dicot plants appear specialized on Clade-A fungi. Cultivar sharing between sympatric leafcutter species occurs frequently such that cultivars of Atta are not distinct from those of Acromyrmex. Leafcutters specialized on Clade-B fungi occur only in South America. Diversity of Clade-A fungi is greatest in South America, but minimal in Central and North America. Maximum cultivar diversity in South America is predicted by the Kusnezov–Fowler hypothesis that leafcutter ants originated in subtropical South America and only dicot-specialized leafcutter ants migrated out of South America, but the cultivar diversity becomes also compatible with a recently proposed hypothesis of a Central American origin by postulating that leafcutter ants acquired novel cultivars many times from other nonleafcutter fungus-growing ants during their migrations from Central America across South America. We evaluate these biogeographic hypotheses in the light of estimated dates for the origins of leafcutter ants and their cultivars

Multi-messenger Observations of a Binary Neutron Star Merger

On 2017 August 17 a binary neutron star coalescence candidate (later designated GW170817) with merger time 12:41:04 UTC was observed through gravitational waves by the Advanced LIGO and Advanced Virgo detectors. The Fermi Gamma-ray Burst Monitor independently detected a gamma-ray burst (GRB 170817A) with a time delay of ∼ 1.7 {{s}} with respect to the merger time. From the gravitational-wave signal, the source was initially localized to a sky region of 31 deg2 at a luminosity distance of {40}-8+8 Mpc and with component masses consistent with neutron stars. The component masses were later measured to be in the range 0.86 to 2.26 {M}⊙ . An extensive observing campaign was launched across the electromagnetic spectrum leading to the discovery of a bright optical transient (SSS17a, now with the IAU identification of AT 2017gfo) in NGC 4993 (at ∼ 40 {{Mpc}}) less than 11 hours after the merger by the One-Meter, Two Hemisphere (1M2H) team using the 1 m Swope Telescope. The optical transient was independently detected by multiple teams within an hour. Subsequent observations targeted the object and its environment. Early ultraviolet observations revealed a blue transient that faded within 48 hours. Optical and infrared observations showed a redward evolution over ∼10 days. Following early non-detections, X-ray and radio emission were discovered at the transient's position ∼ 9 and ∼ 16 days, respectively, after the merger. Both the X-ray and radio emission likely arise from a physical process that is distinct from the one that generates the UV/optical/near-infrared emission. No ultra-high-energy gamma-rays and no neutrino candidates consistent with the source were found in follow-up searches. These observations support the hypothesis that GW170817 was produced by the merger of two neutron stars in NGC 4993 followed by a short gamma-ray burst (GRB 170817A) and a kilonova/macronova powered by the radioactive decay of r-process nuclei synthesized in the ejecta.The AST3 project is supported by the National Basic Research Program (973 Program) of China (Grant Nos. 2013CB834901, 2013CB834900, 2013CB834903), and the Chinese Polar Environment Comprehensive Investigation & Assessment Program (grant No. CHINARE2016-02-03-05). The construction of the AST3 telescopes has received fundings from Tsinghua University, Nanjing University, Beijing Normal University, University of New South Wales, and Texas A&M University, the Australian Antarctic Division, and the National Collaborative Research Infrastructure Strategy (NCRIS) of Australia. It has also received funding from Chinese Academy of Sciences through the Center for Astronomical Mega-Science and National Astronomical Observatory of China (NAOC).The collaboration between LIGO/Virgo and EVN/e-MERLIN is part of a project that has received funding from the European Unions Horizon 2020 research and innovation programme under grant agreement No. 653477.B.C., V.C., A.G., and W.S.P. gratefully acknowledge NASA funding through contract NNM13AA43C. M.S.B., R.H., P.J., C.A.M., S.P., R.D.P., M.S., and P.V. gratefully acknowledge NASA funding from cooperative agreement NNM11AA01A. E.B. is supported by an appointment to the NASA Postdoctoral Program at the Goddard Space Flight Center, administered by Universities Space Research Association under contract with NASA. D.K., C.A.W.H., C.M. H., and J.R. gratefully acknowledge NASA funding through the Fermi-GBM project. Support for the German contribution to GBM was provided by the Bundesministerium für Bildung und Forschung (BMBF) via the Deutsches Zentrum für Luft und Raumfahrt (DLR) under contract number 50 QV 0301. A. v.K. was supported by the Bundesministeriums für Wirtschaft und Technologie (BMWi) through DLR grant 50 OG 1101. S. M.B. acknowledges support from Science Foundation Ireland under grant 12/IP/1288.Part of the funding for GROND was generously granted from the Leibniz-Prize to Prof. G. Hasinger (DFG grant HA 1850/28-1). “We acknowledge the excellent help in obtaining GROND data from Angela Hempel, Markus Rabus and Régis Lachaume on La Silla.

Localization and broadband follow-up of the gravitational-wave transient GW 150914

A gravitational-wave (GW) transient was identified in data recorded by the Advanced Laser Interferometer Gravitational-wave Observatory (LIGO) detectors on 2015 September 14. The event, initially designated G184098 and later given the name GW150914, is described in detail elsewhere. By prior arrangement, preliminary estimates of the time, significance, and sky location of the event were shared with 63 teams of observers covering radio, optical, near-infrared, X-ray, and gamma-ray wavelengths with ground- and space-based facilities. In this Letter we describe the low-latency analysis of the GW data and present the sky localization of the first observed compact binary merger. We summarize the follow-up observations reported by 25 teams via private Gamma-ray Coordinates Network circulars, giving an overview of the participating facilities, the GW sky localization coverage, the timeline, and depth of the observations. As this event turned out to be a binary black hole merger, there is little expectation of a detectable electromagnetic (EM) signature. Nevertheless, this first broadband campaign to search for a counterpart of an Advanced LIGO source represents a milestone and highlights the broad capabilities of the transient astronomy community and the observing strategies that have been developed to pursue neutron star binary merger events. Detailed investigations of the EM data and results of the EM follow-up campaign are being disseminated in papers by the individual teams