Chromosome-level genome assembly and annotation of two lineages of the ant Cataglyphis hispanica: stepping stones towards genomic studies of hybridogenesis and thermal adaptation in desert ants

10.24072/pcjournal.140 - Peer Community Journal, Volume 2 (2022), article no. e40.

Get full text PDF Peer reviewed and recommended by PCI

Cataglyphis are thermophilic ants that forage during the day when temperatures are highest and sometimes close to their critical thermal limit. Several Cataglyphis species have evolved unusual reproductive systems such as facultative queen parthenogenesis or social hybridogenesis, which have not yet been investigated in detail at the molecular level. We generated high-quality genome assemblies for two hybridogenetic lineages of the Iberian ant Cataglyphis hispanica using long-read Nanopore sequencing and exploited chromosome conformation capture (3C) sequencing to assemble contigs into 26 and 27 chromosomes, respectively. Further karyotype analyses confirm this difference in chromosome numbers between lineages; however, they also suggest it may not be fixed among lineages. We obtained transcriptomic data to assist gene annotation and built custom repeat libraries for each of the two assemblies. Comparative analyses with 19 other published ant genomes were also conducted. These new genomic resources pave the way for exploring the genetic mechanisms underlying the remarkable thermal adaptation and the molecular mechanisms associated with transitions between different genetic systems characteristic of the ant genus Cataglyphis.

Published online:
DOI: 10.24072/pcjournal.140
Darras, Hugo 1, 2; De Souza Araujo, Natalia 2, 3; Baudry, Lyam 4, 5; Guiglielmoni, Nadège 2, 6; Lorite, Pedro 7; Marbouty, Martial 5; Rodriguez, Fernando 8; Arkhipova, Irina 8; Koszul, Romain 5; Flot, Jean-François 2, 3; Aron, Serge 2

1 Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland
2 Unit of Evolutionary Biology & Ecology, Université libre de Bruxelles (ULB), Brussels, Belgium
3 Interuniversity Institute of Bioinformatics in Brussels – (IB) Brussels, Belgium
4 Centre for Integrative Genomics, University of Lausanne, Lausanne, Switzerland
5 Unité Régulation Spatiale des Génomes, CNRS, Institut Pasteur, Paris, France
6 Universität zu Köln, Köln, Germany
7 Department of Biologia Experimental, Universidad de Jaén, Jaén, Spain
8 Marine Biological Laboratory, Woods Hole, Massachusetts, USA
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {Darras, Hugo and De Souza Araujo, Natalia and Baudry, Lyam and Guiglielmoni, Nad\`ege and Lorite, Pedro and Marbouty, Martial and Rodriguez, Fernando and Arkhipova, Irina and Koszul, Romain and Flot, Jean-Fran\c{c}ois and Aron, Serge},
     title = {Chromosome-level genome assembly and annotation of two lineages of the ant {<i>Cataglyphis} hispanica</i>: stepping stones towards genomic studies of hybridogenesis and thermal adaptation in desert ants},
     journal = {Peer Community Journal},
     eid = {e40},
     publisher = {Peer Community In},
     volume = {2},
     year = {2022},
     doi = {10.24072/pcjournal.140},
     url = {}
TI  - Chromosome-level genome assembly and annotation of two lineages of the ant <i>Cataglyphis hispanica</i>: stepping stones towards genomic studies of hybridogenesis and thermal adaptation in desert ants
JO  - Peer Community Journal
PY  - 2022
DA  - 2022///
VL  - 2
PB  - Peer Community In
UR  -
UR  -
DO  - 10.24072/pcjournal.140
ID  - 10_24072_pcjournal_140
ER  - 
%0 Journal Article
%T Chromosome-level genome assembly and annotation of two lineages of the ant <i>Cataglyphis hispanica</i>: stepping stones towards genomic studies of hybridogenesis and thermal adaptation in desert ants
%J Peer Community Journal
%D 2022
%V 2
%I Peer Community In
%R 10.24072/pcjournal.140
%F 10_24072_pcjournal_140
Darras, Hugo; De Souza Araujo, Natalia; Baudry, Lyam; Guiglielmoni, Nadège; Lorite, Pedro; Marbouty, Martial; Rodriguez, Fernando; Arkhipova, Irina; Koszul, Romain; Flot, Jean-François; Aron, Serge. Chromosome-level genome assembly and annotation of two lineages of the ant Cataglyphis hispanica: stepping stones towards genomic studies of hybridogenesis and thermal adaptation in desert ants. Peer Community Journal, Volume 2 (2022), article  no. e40. doi : 10.24072/pcjournal.140.

Peer reviewed and recommended by PCI : 10.24072/pci.genomics.100017

[1] Anderson, K.; Linksvayer, T.; Smith, C. The causes and consequences of genetic caste determination in ants (Hymenoptera: Formicidae), Myrmecological News, Volume 11 (2008), pp. 119-132

[2] Aron, S.; Lybaert, P.; Baudoux, C.; Vandervelden, M.; Fournier, D. Sperm production characteristics vary with level of sperm competition in <i>Cataglyphis</i> desert ants, Functional Ecology, Volume 30 (2016) no. 4, pp. 614-624 | DOI

[3] Aron, S.; Mardulyn, P.; Leniaud, L. Evolution of reproductive traits in Cataglyphis desert ants: mating frequency, queen number, and thelytoky, Behavioral Ecology and Sociobiology, Volume 70 (2016) no. 8, pp. 1367-1379 | DOI

[4] Aron, S.; Wehner, R. Cataglyphis, Encyclopedia of Social Insects, Springer International Publishing, Cham, 2021, pp. 217-223 | DOI

[5] Baudry, L.; Guiglielmoni, N.; Marie-Nelly, H.; Cormier, A.; Marbouty, M.; Avia, K.; Mie, Y. L.; Godfroy, O.; Sterck, L.; Cock, J. M.; Zimmer, C.; Coelho, S. M.; Koszul, R. instaGRAAL: chromosome-level quality scaffolding of genomes using a proximity ligation-based scaffolder, Genome Biology, Volume 21 (2020) no. 1 | DOI

[6] Bolger, A. M.; Lohse, M.; Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data, Bioinformatics, Volume 30 (2014) no. 15, pp. 2114-2120 | DOI

[7] Boulay, R.; Aron, S.; Cerdá, X.; Doums, C.; Graham, P.; Hefetz, A.; Monnin, T. Social Life in Arid Environments: The Case Study of <i>Cataglyphis</i> Ants, Annual Review of Entomology, Volume 62 (2017) no. 1, pp. 305-321 | DOI

[8] Cabanettes, F.; Klopp, C. D-GENIES: dot plot large genomes in an interactive, efficient and simple way, PeerJ, Volume 6 (2018) | DOI

[9] Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses, Bioinformatics, Volume 25 (2009) no. 15, pp. 1972-1973 | DOI

[10] Cerdá, X.; Retana, J.; Cros, S. Critical thermal limits in Mediterranean ant species: trade-off between mortality risk and foraging performance, Functional Ecology, Volume 12 (1998) no. 1, pp. 45-55 | DOI

[11] Cohen, P.; Privman, E. Speciation and hybridization in invasive fire ants, BMC Evolutionary Biology, Volume 19 (2019) no. 1 | DOI

[12] Darras, H.; Kuhn, A.; Aron, S. Evolution of hybridogenetic lineages in <i>Cataglyphis</i> ants, Molecular Ecology, Volume 28 (2019) no. 12, pp. 3073-3088 | DOI

[13] Darras, H.; Leniaud, L.; Aron, S. Large-scale distribution of hybridogenetic lineages in a Spanish desert ant, Proceedings of the Royal Society B: Biological Sciences, Volume 281 (2014) no. 1774 | DOI

[14] Davisson, M. T.; Akeson, E. C. Recombination suppression by heterozygous Robertsonian chromosomes in the mouse., Genetics, Volume 133 (1993) no. 3, pp. 649-667 | DOI

[15] Dobin, A.; Davis, C. A.; Schlesinger, F.; Drenkow, J.; Zaleski, C.; Jha, S.; Batut, P.; Chaisson, M.; Gingeras, T. R. STAR: ultrafast universal RNA-seq aligner, Bioinformatics, Volume 29 (2013) no. 1, pp. 15-21 | DOI

[16] Drăgan, M.-A.; Moghul, I.; Priyam, A.; Bustos, C.; Wurm, Y. GeneValidator: identify problems with protein-coding gene predictions, Bioinformatics, Volume 32 (2016) no. 10, pp. 1559-1561 | DOI

[17] Edgar, R. C. Search and clustering orders of magnitude faster than BLAST, Bioinformatics, Volume 26 (2010) no. 19, pp. 2460-2461 | DOI

[18] Eyer, P. A.; Leniaud, L.; Darras, H.; Aron, S. Hybridogenesis through thelytokous parthenogenesis in two <i> <scp>C</scp> ataglyphis </i> desert ants, Molecular Ecology, Volume 22 (2013) no. 4, pp. 947-955 | DOI

[19] Ellinghaus, D.; Kurtz, S.; Willhoeft, U. LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons, BMC Bioinformatics, Volume 9 (2008) no. 1 | DOI

[20] Emms, D. M.; Kelly, S. OrthoFinder: phylogenetic orthology inference for comparative genomics, Genome Biology, Volume 20 (2019) no. 1 | DOI

[21] Faria, R.; Navarro, A. Chromosomal speciation revisited: rearranging theory with pieces of evidence, Trends in Ecology &amp; Evolution, Volume 25 (2010) no. 11, pp. 660-669 | DOI

[22] Flot, J.-F.; Marie-Nelly, H.; Koszul, R. Contact genomics: scaffolding and phasing (meta)genomes using chromosome 3D physical signatures, FEBS Letters, Volume 589 (2015) no. 20PartA, pp. 2966-2974 | DOI

[23] Flutre, T.; Duprat, E.; Feuillet, C.; Quesneville, H. Considering Transposable Element Diversification in De Novo Annotation Approaches, PLoS ONE, Volume 6 (2011) no. 1 | DOI

[24] Garrison E. , and G. Marth . 2012. “Haplotype-based variant detection from short-read sequencing.” ArXiv.

[25] Gehring, W. J.; Wehner, R. Heat shock protein synthesis and thermotolerance in Cataglyphis, an ant from the Sahara desert., Proceedings of the National Academy of Sciences, Volume 92 (1995) no. 7, pp. 2994-2998 | DOI

[26] Grabherr, M. G.; Haas, B. J.; Yassour, M.; Levin, J. Z.; Thompson, D. A.; Amit, I.; Adiconis, X.; Fan, L.; Raychowdhury, R.; Zeng, Q.; Chen, Z.; Mauceli, E.; Hacohen, N.; Gnirke, A.; Rhind, N.; di Palma, F.; Birren, B. W.; Nusbaum, C.; Lindblad-Toh, K.; Friedman, N.; Regev, A. Full-length transcriptome assembly from RNA-Seq data without a reference genome, Nature Biotechnology, Volume 29 (2011) no. 7, pp. 644-652 | DOI

[27] Gremme, G.; Brendel, V.; Sparks, M. E.; Kurtz, S. Engineering a software tool for gene structure prediction in higher organisms, Information and Software Technology, Volume 47 (2005) no. 15, pp. 965-978 | DOI

[28] Haas, B. J. Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies, Nucleic Acids Research, Volume 31 (2003) no. 19, pp. 5654-5666 | DOI

[29] Haas, B. J.; Papanicolaou, A.; Yassour, M.; Grabherr, M.; Blood, P. D.; Bowden, J.; Couger, M. B.; Eccles, D.; Li, B.; Lieber, M.; MacManes, M. D.; Ott, M.; Orvis, J.; Pochet, N.; Strozzi, F.; Weeks, N.; Westerman, R.; William, T.; Dewey, C. N.; Henschel, R.; LeDuc, R. D.; Friedman, N.; Regev, A. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis, Nature Protocols, Volume 8 (2013) no. 8, pp. 1494-1512 | DOI

[30] Haas, B. J.; Salzberg, S. L.; Zhu, W.; Pertea, M.; Allen, J. E.; Orvis, J.; White, O.; Buell, C. R.; Wortman, J. R. Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments, Genome Biology, Volume 9 (2008) no. 1 | DOI

[31] Hauschteck-Jungen, E.; Jungen, H. Ant chromosomes, Insectes Sociaux, Volume 30 (1983) no. 2, pp. 149-164 | DOI

[32] Hoff, K. J.; Lange, S.; Lomsadze, A.; Borodovsky, M.; Stanke, M. BRAKER1: Unsupervised RNA-Seq-Based Genome Annotation with GeneMark-ET and AUGUSTUS: Table 1., Bioinformatics, Volume 32 (2016) no. 5, pp. 767-769 | DOI

[33] Hoff, K. J.; Lomsadze, A.; Borodovsky, M.; Stanke, M. Whole-Genome Annotation with BRAKER, Methods in Molecular Biology, Springer New York, New York, NY, 2019, pp. 65-95 | DOI

[34] Hoff, K. J.; Lomsadze, A.; Borodovsky, M.; Stanke, M. Whole-Genome Annotation with BRAKER, Methods in Molecular Biology, Springer New York, New York, NY, 2019, pp. 65-95 | DOI

[35] Huerta-Cepas, J.; Szklarczyk, D.; Heller, D.; Hernández-Plaza, A.; Forslund, S. K.; Cook, H.; Mende, D. R.; Letunic, I.; Rattei, T.; Jensen, L. J.; von Mering, C.; Bork, P. eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses, Nucleic Acids Research, Volume 47 (2019) no. D1 | DOI

[36] Hughes, W. O. H.; Boomsma, J. J. Genetic royal cheats in leaf-cutting ant societies, Proceedings of the National Academy of Sciences, Volume 105 (2008) no. 13, pp. 5150-5153 | DOI

[37] Imai, B. H. T.; Urbani, C. B.; Kubota, M.; Sharma, G. P.; Narasimhanna, M. N.; Das, B. C.; Sharma, A. K.; Sharma, A.; Deodikar, G. B.; Vaidya, V. G.; Rajasekarasetty, M. R. Karyological survey of Indian ants., The Japanese Journal of Genetics, Volume 59 (1984) no. 1, pp. 1-32 | DOI

[38] Katoh, K.; Standley, D. M. MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability, Molecular Biology and Evolution, Volume 30 (2013) no. 4, pp. 772-780 | DOI

[39] Keightley, P. D.; Ness, R. W.; Halligan, D. L.; Haddrill, P. R. Estimation of the Spontaneous Mutation Rate per Nucleotide Site in a iDrosophila melanogaster/i Full-Sib Family, Genetics, Volume 196 (2014) no. 1, pp. 313-320 | DOI

[40] Keightley, P. D.; Pinharanda, A.; Ness, R. W.; Simpson, F.; Dasmahapatra, K. K.; Mallet, J.; Davey, J. W.; Jiggins, C. D. Estimation of the Spontaneous Mutation Rate in Heliconius melpomene, Molecular Biology and Evolution, Volume 32 (2014) no. 1, pp. 239-243 | DOI

[41] Kolmogorov, M.; Yuan, J.; Lin, Y.; Pevzner, P. A. Assembly of long, error-prone reads using repeat graphs, Nature Biotechnology, Volume 37 (2019) no. 5, pp. 540-546 | DOI

[42] Konorov, E. A.; Nikitin, M. A.; Mikhailov, K. V.; Lysenkov, S. N.; Belenky, M.; Chang, P. L.; Nuzhdin, S. V.; Scobeyeva, V. A. Genomic exaptation enables Lasius niger adaptation to urban environments, BMC Evolutionary Biology, Volume 17 (2017) no. S1 | DOI

[43] Kuhn, A.; Darras, H.; Paknia, O.; Aron, S. Repeated evolution of queen parthenogenesis and social hybridogenesis in iCataglyphis/i desert ants, Molecular Ecology, Volume 29 (2020) no. 3, pp. 549-564 | DOI

[44] Leniaud, L.; Darras, H.; Boulay, R.; Aron, S. Social Hybridogenesis in the Clonal Ant Cataglyphis hispanica, Current Biology, Volume 22 (2012) no. 13, pp. 1188-1193 | DOI

[45] Lenoir, A. N. E.; Querard, L.; Pondicq, N.; Delalande C. Habitat exploitation and intercolonial relationships in the ant Cataglyphis cursor (Hymenoptera: Formicidae), Acta Oecologica, Volume 11 (1990), pp. 3-18

[46] Li, H.; Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform, Bioinformatics, Volume 25 (2009) no. 14, pp. 1754-1760 | DOI

[47] Li, H.; Handsaker, B.; Wysoker, A.; Fennell, T.; Ruan, J.; Homer, N.; Marth, G.; Abecasis, G.; Durbin, R. The Sequence Alignment/Map format and SAMtools, Bioinformatics, Volume 25 (2009) no. 16, pp. 2078-2079 | DOI

[48] Lieberman-Aiden, E.; van Berkum, N. L.; Williams, L.; Imakaev, M.; Ragoczy, T.; Telling, A.; Amit, I.; Lajoie, B. R.; Sabo, P. J.; Dorschner, M. O.; Sandstrom, R.; Bernstein, B.; Bender, M. A.; Groudine, M.; Gnirke, A.; Stamatoyannopoulos, J.; Mirny, L. A.; Lander, E. S.; Dekker, J. Comprehensive Mapping of Long-Range Interactions Reveals Folding Principles of the Human Genome, Science, Volume 326 (2009) no. 5950, pp. 289-293 | DOI

[49] Lin, H.-N.; Hsu, W.-L. MapCaller – An integrated and efficient tool for short-read mapping and variant calling using high-throughput sequenced data, bioRxiv, 783605, | DOI

[50] Linksvayer, T. A.; Busch, J. W.; Smith, C. R. Social supergenes of superorganisms: Do supergenes play important roles in social evolution?, BioEssays, Volume 35 (2013) no. 8, pp. 683-689 | DOI

[51] Liu, H.; Jia, Y.; Sun, X.; Tian, D.; Hurst, L. D.; Yang, S. Direct Determination of the Mutation Rate in the Bumblebee Reveals Evidence for Weak Recombination-Associated Mutation and an Approximate Rate Constancy in Insects, Molecular Biology and Evolution, Volume 34 (2017) no. 1, pp. 119-130 | DOI

[52] Lorite, P.; Chica, E.; Palomeque, T. Cytogenetic studies of antiLinepithema humile/iShattuck (=iIridomyrmex humilis/iMayr) in European populations, Caryologia, Volume 49 (1996) no. 2, pp. 199-205 | DOI

[53] Lorite, P.; Palomeque, T. Karyotype evolution in ants (Hymenoptera: Formicidae), with a review of the known ant chromosome numbers, Myrmecological News, Volume 13 (2010), pp. 89-102

[54] Manni, M.; Berkeley, M. R.; Seppey, M.; Simão, F. A.; Zdobnov, E. M. BUSCO Update: Novel and Streamlined Workflows along with Broader and Deeper Phylogenetic Coverage for Scoring of Eukaryotic, Prokaryotic, and Viral Genomes, Molecular Biology and Evolution, Volume 38 (2021) no. 10, pp. 4647-4654 | DOI

[55] Mapleson, D.; Garcia Accinelli, G.; Kettleborough, G.; Wright, J.; Clavijo, B. J. KAT: a K-mer analysis toolkit to quality control NGS datasets and genome assemblies, Bioinformatics, Volume 33 (2016) | DOI

[56] Marie-Nelly, H.; Marbouty, M.; Cournac, A.; Flot, J.-F.; Liti, G.; Parodi, D. P.; Syan, S.; Guillén, N.; Margeot, A.; Zimmer, C.; Koszul, R. High-quality genome (re)assembly using chromosomal contact data, Nature Communications, Volume 5 (2014) no. 1 | DOI

[57] Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads, EMBnet.journal, Volume 17 (2011) no. 1 | DOI

[58] Matthey-Doret C. , L. Baudry , A. Bignaud , A. Cournac , R. Montagne , N. Guiglielmoni , T. Foutel-Rodier , and V.F. Scolari . 2020. “hicstuff: Simple library/pipeline to generate and handle Hi-C data”. Zenodo.

[59] Nguyen, L.-T.; Schmidt, H. A.; von Haeseler, A.; Minh, B. Q. IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies, Molecular Biology and Evolution, Volume 32 (2015) no. 1, pp. 268-274 | DOI

[60] Obbard, D. J.; Maclennan, J.; Kim, K.-W.; Rambaut, A.; O’Grady, P. M.; Jiggins, F. M. Estimating Divergence Dates and Substitution Rates in the Drosophila Phylogeny, Molecular Biology and Evolution, Volume 29 (2012) no. 11, pp. 3459-3473 | DOI

[61] Oppold, A.-M.; Pfenninger, M. Direct estimation of the spontaneous mutation rate by short-term mutation accumulation lines in iChironomus riparius/i, Evolution Letters, Volume 1 (2017) no. 2, pp. 86-92 | DOI

[62] Pearcy, M.; Hardy, O. J.; Aron, S. Automictic parthenogenesis and rate of transition to homozygosity, Heredity, Volume 107 (2011) no. 2, pp. 187-188 | DOI

[63] Pearcy, M.; Aron, S.; Doums, C.; Keller, L. Conditional Use of Sex and Parthenogenesis for Worker and Queen Production in Ants, Science, Volume 306 (2004) no. 5702, pp. 1780-1783 | DOI

[64] Perez, R.; Aron, S. Adaptations to thermal stress in social insects: recent advances and future directions, Biological Reviews, Volume 95 (2020) no. 6, pp. 1535-1553 | DOI

[65] Perez, R.; Souza Araujo, N.; Defrance, M.; Aron, S. Molecular adaptations to heat stress in the thermophilic ant genus iCataglyphis/i, Molecular Ecology, Volume 30 (2021) no. 21, pp. 5503-5516 | DOI

[66] Pfeffer, S. E.; Wahl, V. L.; Wittlinger, M.; Wolf, H. High-speed locomotion in the Saharan silver ant, iCataglyphis bombycina/i, Journal of Experimental Biology, Volume 222 (2019) no. 20 | DOI

[67] Quesneville, H.; Bergman, C. M.; Andrieu, O.; Autard, D.; Nouaud, D.; Ashburner, M.; Anxolabehere, D. Combined Evidence Annotation of Transposable Elements in Genome Sequences, PLoS Computational Biology, Volume 1 (2005) no. 2 | DOI

[68] Sanderson, M. J. r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock, Bioinformatics, Volume 19 (2003) no. 2, pp. 301-302 | DOI

[69] Schrader, L.; Kim, J. W.; Ence, D.; Zimin, A.; Klein, A.; Wyschetzki, K.; Weichselgartner, T.; Kemena, C.; Stökl, J.; Schultner, E.; Wurm, Y.; Smith, C. D.; Yandell, M.; Heinze, J.; Gadau, J.; Oettler, J. Transposable element islands facilitate adaptation to novel environments in an invasive species, Nature Communications, Volume 5 (2014) no. 1 | DOI

[70] Schwander, T.; Libbrecht, R.; Keller, L. Supergenes and Complex Phenotypes, Current Biology, Volume 24 (2014) no. 7 | DOI

[71] Shumate, A.; Salzberg, S. L. Liftoff: accurate mapping of gene annotations, Bioinformatics, Volume 37 (2021) no. 12, pp. 1639-1643 | DOI

[72] Simão, F. A.; Waterhouse, R. M.; Ioannidis, P.; Kriventseva, E. V.; Zdobnov, E. M. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs, Bioinformatics, Volume 31 (2015) no. 19, pp. 3210-3212 | DOI

[73] Sommer, S.; Wehner, R. Leg allometry in ants: Extreme long-leggedness in thermophilic species, Arthropod Structure amp; Development, Volume 41 (2012) no. 1, pp. 71-77 | DOI

[74] Waterhouse, R. M.; Seppey, M.; Simão, F. A.; Manni, M.; Ioannidis, P.; Klioutchnikov, G.; Kriventseva, E. V.; Zdobnov, E. M. BUSCO Applications from Quality Assessments to Gene Prediction and Phylogenomics, Molecular Biology and Evolution, Volume 35 (2017) no. 3, pp. 543-548 | DOI

[75] Wehner, R.; Marsh, A. C.; Wehner, S. Desert ants on a thermal tightrope, Nature, Volume 357 (1992) no. 6379, pp. 586-587 | DOI

[76] Weyna, A.; Romiguier, J.; Mullon, C. Hybridization enables the fixation of selfish queen genotypes in eusocial colonies, Evolution Letters, Volume 5 (2021) no. 6, pp. 582-594 | DOI

[77] Willot, Q.; Gueydan, C.; Aron, S. Proteome stability, heat hardening, and heat-shock protein expression profiles in iCataglyphis/i desert ants, Journal of Experimental Biology, Volume 270 (2017), pp. 1721-1728 | DOI

[78] Withrow, J. M.; Tarpy, D. R. Cryptic “royal” subfamilies in honey bee (Apis mellifera) colonies, PLOS ONE, Volume 13 (2018) no. 7 | DOI

[79] Xu, M.; Guo, L.; Gu, S.; Wang, O.; Zhang, R.; Fan, G.; Xu, X.; Deng, L.; Liu, X. TGS-GapCloser: fast and accurately passing through the Bermuda in large genome using error-prone third-generation long reads, bioRxiv, 831248, | DOI

[80] Yahav, T.; Privman, E. A comparative analysis of methods for de novo assembly of hymenopteran genomes using either haploid or diploid samples, Scientific Reports, Volume 9 (2019) no. 1 | DOI

[81] Yang, S.; Wang, L.; Huang, J.; Zhang, X.; Yuan, Y.; Chen, J.-Q.; Hurst, L. D.; Tian, D. Parent–progeny sequencing indicates higher mutation rates in heterozygotes, Nature, Volume 523 (2015) no. 7561, pp. 463-467 | DOI

Cited by Sources: