Genomic exaptation enables Lasius niger adaptation to urban environments

Abstract

BackgroundThe world is rapidly urbanizing, and only a subset of species are able to succeed in stressful city environments. Efficient genome-enabled stress response appears to be a likely prerequisite for urban adaptation. Despite the important role ants play in the ecosytem, only the genomes of ~13 have been sequenced so far. Here, we present the draft genome assembly of the black garden ant Lasius niger – the most successful urban inhabitant of all ants – and we compare it with the genomes of other ant species, including the closely related Camponotus floridanus.ResultsSequences from 272 M Illumina reads were assembled into 41,406 contigs with total length of 245 MB, and N50 of 16,382 bp, similar to other ant genome assemblies enabling comparative genomic analysis. Remarkably, the predicted proteome of L. niger is significantly enriched relative to other ant genomes in terms of abundance of domains involved in nucleic acid binding, DNA repair, and nucleotidyl transferase activity, reflecting transposable element proliferation and a likely genomic response. With respect to environmental stress, we note a proliferation of various detoxification genes, including glutatione-S-transferases and those in the cytochrome P450 families. Notably, the CYP9 family is highly expanded with 19 complete and 21 nearly complete members - over twice as many compared to other ants. This family exhibits the signatures of strong directional selection, with eleven positively selected positions in ligand-binding pockets of enzymes. Gene family contraction was detected for several components of the olfactory system, accompanied by instances of both directional selection and relaxation.ConclusionsOur results suggest that the success of L. niger in urbanized areas may be the result of fortuitous coincidence of several factors, including the expansion of the CYP9 cytochrome family due to coevolution with parasitic fungi, the diversification of DNA repair systems as an answer to proliferation of retroelements, and the reduction of olfactory system and behavioral preadaptations from non-territorial subdominant life strategies found in natural environments. Diversification of cytochromes and DNA repair systems along with reduced odorant communication are the basis of L. niger pollutant resistance and polyphagy, while non-territorial and mobilization strategies allows more efficient exploitation of large but patchy food sources.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0867-x) contains supplementary material, which is available to authorized users.

Gene expression is more strongly influenced by age than caste in the ant Lasius niger

“…Annotation of these sequences using blastx revealed that one of these genes is a Cytochrome P450 (CYP) reductase. Expansion of CYPs and sequence evolution in this family has been suggested to be linked with the success of L. niger in urban environments (Konorov et al., ).…”

Comparative transcriptomics of social insect queen pheromones

“…We aligned and quantified the raw reads using the RSEM 64 pipeline with Bowtie2 65 to transcripts from published genomes for A. mellifera , B. terrestris and L. niger 66–68 . The L. niger genome assembly had no isoform information, so we identified isoforms using Tophat 69 .…”

Transcriptome sequencing reveals high isoform diversity in the ant Formica exsecta

“…Contigs annotated with known micro-organisms, and probable parasites such as viruses and fungi, were first filtered out from the data as exogenous material, as described in Johansson et al (2013) , and this exogenous material has now been made available in NCBI database (Bioproject: PRJNA412141 ). The remaining contigs were then aligned (BLASTx, e -value threshold 10 −3 ) to (a) the predicted gene sets of published ant genomes available on the Fourmidable database, including the closest species such as Camponotus floridanus , Lasius niger, as well as more distantly related species such as Cerapachys biroi , Linepithema humile , Solenopsis invicta , Vollenhovia emeryi , Wasmannia auropunctata , Pogonomyrmex barbatus , Monomorium pharaonis , Harpegnathos saltator , Acromyrmex echinatior and Atta cephalotes ( Wurm et al, 2011 ; Wurm et al, 2009 ; Bonasio et al, 2010 ; Suen et al, 2011 ; Smith et al, 2011a ; Smith et al, 2011b ; Nygaard et al, 2011 ; Gadau et al, 2012 ; Oxley et al, 2014 ; Schrader et al, 2014 ; Konorov et al, 2017 ), (b) the honey bee genome ( Weinstock et al, 2006 ), (c) the predicted gene sets of Nasonia vitripennis , Tribolium castaneum ( Wurm et al, 2009 ), and Drosophila melanogaster ( Gramates et al, 2017 ), (d) as well as non-redundant (NR) protein datasets available in the NCBI database (Updated 2015, Updated 2017) for insect species. A minimum requirement of 70% amino acid identity, and at least 100 bases (33 amino acids) alignment length was used.…”

“…Current genomic resources of social insects are available for important pollinators such as honey bees and bumble bees ( Colgan et al, 2011 ; Kocher et al, 2013 ; Elsik et al, 2014 ; Elsik et al, 2016 ; Kapheim et al, 2015 ; Sadd et al, 2015 ), and primitively eusocial paper wasps ( Sumner, Pereboom & Jordan, 2006 ; Ferreira et al, 2013 ). For ants, genome sequences are currently available for 13, and transcriptomes for 23, species in the Fourmidable database ( Wurm et al, 2009 ), including well studied species such as the invasive argentine ant (Linepithema humile) , the fire ant (Solenopsis invicta), and the leaf cutting ant species (Acromyrmex echinatior and Atta cephalotes ( Bonasio et al, 2010 ; Suen et al, 2011 ; Smith et al, 2011a ; Smith et al, 2011b ; Wurm et al, 2011 ; Nygaard et al, 2011 ; Gadau et al, 2012 ; Oxley et al, 2014 ; Schrader et al, 2014 ; Konorov et al, 2017 ). However, these data cover only a fraction of the genetic richness of the more than 11,000 described ant species, and over 100 million years of evolution ( Wilson & Hölldobler, 2005 ).…”