Section: Evolutionary Biology
Topic: Evolution, Genetics/Genomics, Population biology

Relaxation of purifying selection suggests low effective population size in eusocial Hymenoptera and solitary pollinating bees

Weyna, Arthur1; Romiguier, Jonathan1  
1 Institut des Sciences de l’Evolution (UMR 5554), University of Montpellier, CNRS – Montpellier, France

Corresponding author(s): Romiguier, Jonathan ()

10.24072/pcjournal.3 - Peer Community Journal, Volume 1 (2021), article no. e2.

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With one of the highest number of parasite, eusocial and pollinator species among all insect orders, Hymenoptera features a great diversity of specific lifestyles. At the population genetic level, such life-history strategies are expected to decrease effective population size and efficiency of purifying selection. In this study, we tested this hypothesis by estimating the relative rate of non-synonymous substitution in 169 species to investigate the variation in natural selection efficiency throughout the hymenopteran tree of life. We found no effect of parasitism or body size, but show that relaxed selection is associated with eusociality, suggesting that the division of reproductive labour decreases effective population size in ants, bees and wasps. Unexpectedly, the effect of eusociality is marginal compared to a striking and widespread relaxation of selection in both social and non social bees, which indicates that these keystone pollinator species generally feature low effective population sizes. This widespread pattern suggests specific constraints in pollinating bees potentially linked to limited resource and high parental investment. The particularly high load of deleterious mutations we report in the genome of these crucial ecosystem engineer species also raises new concerns about their ongoing population decline.
Published online:
DOI: 10.24072/pcjournal.3
Type: Research article

Weyna, Arthur 1; Romiguier, Jonathan 1

1 Institut des Sciences de l’Evolution (UMR 5554), University of Montpellier, CNRS – Montpellier, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights 
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Weyna, Arthur; Romiguier, Jonathan. Relaxation of purifying selection suggests low effective population size in eusocial Hymenoptera and solitary pollinating bees. Peer Community Journal, Volume 1 (2021), article  no. e2. doi : 10.24072/pcjournal.3. https://peercommunityjournal.org/articles/10.24072/pcjournal.3/

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.evolbiol.100120

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The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Alexa, A.; Rahnenfuhrer, J. topGO: Enrichment analysis for gene ontology. R package version 2.42.0.

[2] Arbetman, M. P.; Gleiser, G.; Morales, C. L.; Williams, P.; Aizen, M. A. Global decline of bumblebees is phylogenetically structured and inversely related to species range size and pathogen incidence, Proceedings of the Royal Society B: Biological Sciences, Volume 284 (2017) no. 1859 | DOI

[3] Asplen, M. K.; Whitfield, J. B.; De Boer, J. G.; Heimpel, G. E. Ancestral state reconstruction analysis of hymenopteran sex determination mechanisms, Journal of Evolutionary Biology, Volume 22 (2009) no. 8, pp. 1762-1769 | DOI

[4] Berkelhamer, R. C. Intraspecific Genetic Variation and Haplodiploidy, Eusociality, and Polygyny in the Hymenoptera, Evolution, Volume 37 (1983) no. 3, pp. 540-545 | DOI

[5] Bonasio, R.; Zhang, G.; Ye, C.; Mutti, N. S.; Fang, X.; Qin, N.; Donahue, G.; Yang, P.; Li, Q.; Li, C.; Zhang, P.; Huang, Z.; Berger, S. L.; Reinberg, D.; Wang, J.; Liebig, J. enomic comparison of the ants Harpegnathos saltator and Camponotus floridanus, Science, Volume 329 (2010) no. 5995, pp. 1068-1071 | DOI

[6] Botero-Castro, F.; Figuet, E.; Tilak, M.-K.; Nabholz, B.; Galtier, N. Avian Genomes Revisited: Hidden Genes Uncovered and the Rates versus Traits Paradox in Birds, Molecular Biology and Evolution, Volume 34 (2017) no. 12, pp. 3123-3131 | DOI

[7] Bourke, A. Colony size, social complexity and reproductive conflict in social insects, Journal of Evolutionary Biology, Volume 12 (1999) no. 2, pp. 245-257 | DOI

[8] Bromham, L.; Leys, R. Sociality and the Rate of Molecular Evolution, Molecular Biology and Evolution, Volume 22 (2005) no. 6, pp. 1393-1402 | DOI

[9] Di Franco, A.; Poujol, R.; Baurain, D.; Philippe, H. Evaluating the usefulness of alignment filtering methods to reduce the impact of errors on evolutionary inferences, BMC Evolutionary Biology, Volume 19 (2019) | DOI

[10] Duret, L.; Galtier, N. Biased Gene Conversion and the Evolution of Mammalian Genomic Landscapes, Annual Review of Genomics and Human Genetics, Volume 10 (2009) no. 1, pp. 285-311 | DOI

[11] Dutheil, J.; Boussau, B. Non-homogeneous models of sequence evolution in the Bio++ suite of libraries and programs, BMC Evolutionary Biology, Volume 8 (2008) | DOI

[12] Felsenstein, J. Phylogenies and the Comparative Method, The American Naturalist, Volume 125 (1985) no. 1, pp. 1-15 | DOI

[13] Figuet, E.; Nabholz, B.; Bonneau, M.; Mas Carrio, E.; Nadachowska-Brzyska, K.; Ellegren, H.; Galtier, N. Life History Traits, Protein Evolution, and the Nearly Neutral Theory in Amniotes, Molecular Biology and Evolution, Volume 33 (2016) no. 6, pp. 1517-1527 | DOI

[14] Galtier, N.; Roux, C.; Rousselle, M.; Romiguier, J.; Figuet, E.; Glémin, S.; Bierne, N.; Duret, L. Codon Usage Bias in Animals: Disentangling the Effects of Natural Selection, Effective Population Size, and GC-Biased Gene Conversion, Molecular Biology and Evolution, Volume 35 (2018) no. 5, pp. 1092-1103 | DOI

[15] Guéguen, L.; Duret, L. Unbiased Estimate of Synonymous and Nonsynonymous Substitution Rates with Nonstationary Base Composition, Molecular Biology and Evolution, Volume 35 (2017) no. 3, pp. 734-742 | DOI

[16] Hamilton, W. The genetical evolution of social behaviour. I, Journal of Theoretical Biology, Volume 7 (1964) no. 1, pp. 1-16 | DOI

[17] Hölldobler, B.; Wilson, E. O. The Ants, Springer Berlin Heidelberg, Berlin, Heidelberg, 1990 | DOI

[18] Hughes, W. O. H.; Oldroyd, B. P.; Beekman, M.; Ratnieks, F. L. W. Ancestral Monogamy Shows Kin Selection Is Key to the Evolution of Eusociality, Science, Volume 320 (2008) no. 5880, pp. 1213-1216 | DOI

[19] Husseneder, C.; Brandl, R.; Epplen, J.; Epplen, J.; Kaib, M. Within-Colony Relatedness in a Termite Species: Genetic Roads to Eusociality?, Behaviour, Volume 136 (1999) no. 9, pp. 1045-1063 | DOI

[20] Imrit, M. A.; Dogantzis, K. A.; Harpur, B. A.; Zayed, A. Eusociality influences the strength of negative selection on insect genomes, Proceedings of the Royal Society B: Biological Sciences, Volume 287 (2020) no. 1933 | DOI

[21] JERVIS, M.; FERNS, P. Towards a general perspective on life-history evolution and diversification in parasitoid wasps, Biological Journal of the Linnean Society, Volume 104 (2011) no. 2, pp. 443-461 | DOI

[22] Jones, J. C.; Wallberg, A.; Christmas, M. J.; Kapheim, K. M.; Webster, M. T. Extreme Differences in Recombination Rate between the Genomes of a Solitary and a Social Bee, Molecular Biology and Evolution, Volume 36 (2019) no. 10, pp. 2277-2291 | DOI

[23] Kay, T.; Keller, L.; Lehmann, L. The evolution of altruism and the serial rediscovery of the role of relatedness, Proceedings of the National Academy of Sciences, Volume 117 (2020) no. 46, pp. 28894-28898 | DOI

[24] Keller, L.; Genoud, M. Extraordinary lifespans in ants: a test of evolutionary theories of ageing, Nature, Volume 389 (1997) no. 6654, pp. 958-960 | DOI

[25] Lartillot, N. Phylogenetic Patterns of GC-Biased Gene Conversion in Placental Mammals and the Evolutionary Dynamics of Recombination Landscapes, Molecular Biology and Evolution, Volume 30 (2012) no. 3, pp. 489-502 | DOI

[26] Mayhew, P. J. Comparing parasitoid life histories, Entomologia Experimentalis et Applicata, Volume 159 (2016) no. 2, pp. 147-162 | DOI

[27] Mazé-Guilmo, E.; Blanchet, S.; McCoy, K. D.; Loot, G. Host dispersal as the driver of parasite genetic structure: a paradigm lost?, Ecology Letters, Volume 19 (2016) no. 3, pp. 336-347 | DOI

[28] Murray, T. E.; Kuhlmann, M.; Potts, S. G. Conservation ecology of bees: populations, species and communities, Apidologie, Volume 40 (2009) no. 3, pp. 211-236 | DOI

[29] Nikolaev, S. I.; Montoya-Burgos, J. I.; Popadin, K.; Parand, L.; Margulies, E. H.; Antonarakis, S. E. Life-history traits drive the evolutionary rates of mammalian coding and noncoding genomic elements, Proceedings of the National Academy of Sciences, Volume 104 (2007) no. 51, pp. 20443-20448 | DOI

[30] Nowak, M. A.; Tarnita, C. E.; Wilson, E. O. The evolution of eusociality, Nature, Volume 466 (2010) no. 7310, pp. 1057-1062 | DOI

[31] Nygaard, S.; Zhang, G.; Schiøtt, M.; Li, C.; Wurm, Y.; Hu, H.; Zhou, J.; Ji, L.; Qiu, F.; Rasmussen, M.; Pan, H.; Hauser, F.; Krogh, A.; Grimmelikhuijzen, C. J.; Wang, J.; Boomsma, J. J. The genome of the leaf-cutting ant Acromyrmex echinatior suggests key adaptations to advanced social life and fungus farming, Genome Research, Volume 21 (2011) no. 8, pp. 1339-1348 | DOI

[32] Orr, M. C.; Hughes, A. C.; Chesters, D.; Pickering, J.; Zhu, C.-D.; Ascher, J. S. Global Patterns and Drivers of Bee Distribution, Current Biology, Volume 31 (2020) no. 3, pp. 451-458 | DOI

[33] Owen, R. E. Difficulties With the Interpretation of Patterns of Genetic Variation in the Eusocial Hymenoptera, Evolution, Volume 39 (1985) no. 1, pp. 205-210 | DOI

[34] Papkou, A.; Gokhale, C. S.; Traulsen, A.; Schulenburg, H. Host–parasite coevolution: why changing population size matters, Zoology, Volume 119 (2016) no. 4, pp. 330-338 | DOI

[35] Paradis, E.; Schliep, K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R, Bioinformatics, Volume 35 (2018) no. 3, pp. 526-528 | DOI

[36] Peters, R. S.; Krogmann, L.; Mayer, C.; Donath, A.; Gunkel, S.; Meusemann, K.; Kozlov, A.; Podsiadlowski, L.; Petersen, M.; Lanfear, R.; Diez, P. A.; Heraty, J.; Kjer, K. M.; Klopfstein, S.; Meier, R.; Polidori, C.; Schmitt, T.; Liu, S.; Zhou, X.; Wappler, T.; Rust, J.; Misof, B.; Niehuis, O. Evolutionary History of the Hymenoptera, Current Biology, Volume 27 no. 7, pp. 1013-1018 | DOI

[37] Philippe, H.; Vienne, D. M. d.; Ranwez, V.; Roure, B.; Baurain, D.; Delsuc, F. Pitfalls in supermatrix phylogenomics, European Journal of Taxonomy (2017) no. 283, pp. 1-25 | DOI

[38] Pond, S. L. K.; Frost, S. D. W.; Muse, S. V. HyPhy: hypothesis testing using phylogenies, Bioinformatics, Volume 21 (2004) no. 5, pp. 676-679 | DOI

[39] Popadin, K.; Polishchuk, L. V.; Mamirova, L.; Knorre, D.; Gunbin, K. Accumulation of slightly deleterious mutations in mitochondrial protein-coding genes of large versus small mammals, Proceedings of the National Academy of Sciences, Volume 104 (2007) no. 33, pp. 13390-13395 | DOI

[40] Powney, G. D.; Carvell, C.; Edwards, M.; Morris, R. K. A.; Roy, H. E.; Woodcock, B. A.; Isaac, N. J. B. Widespread losses of pollinating insects in Britain, Nature Communications, Volume 10 (2019) no. 1 | DOI

[41] Rabeling, C.; Kronauer, D. J. Thelytokous Parthenogenesis in Eusocial Hymenoptera, Annual Review of Entomology, Volume 58 (2012) no. 1, pp. 273-292 | DOI

[42] Ranwez, V.; Harispe, S.; Delsuc, F.; Douzery, E. J. P. MACSE: Multiple Alignment of Coding SEquences Accounting for Frameshifts and Stop Codons, PLoS ONE, Volume 6 (2011) no. 9 | DOI

[43] Reeve, H. K.; Reeve, J. S.; Pfennig, D. W. Eusociality and Genetic Variability: A Re-Evaluation, Evolution, Volume 39 (1985) no. 1, pp. 200-201 | DOI

[44] Rolland, J.; Schluter, D.; Romiguier, J. Vulnerability to Fishing and Life History Traits Correlate with the Load of Deleterious Mutations in Teleosts, Molecular Biology and Evolution, Volume 37 (2020) no. 8, pp. 2192-2196 | DOI

[45] Romiguier, J.; Ranwez, V.; Douzery, E.; Galtier, N. Genomic Evidence for Large, Long-Lived Ancestors to Placental Mammals, Molecular Biology and Evolution, Volume 30 (2012) no. 1, pp. 5-13 | DOI

[46] Romiguier, J.; Gayral, P.; Ballenghien, M.; Bernard, A.; Cahais, V.; Chenuil, A.; Chiari, Y.; Dernat, R.; Duret, L.; Faivre, N.; Loire, E.; Lourenco, J. M.; Nabholz, B.; Roux, C.; Tsagkogeorga, G.; Weber, A. A.-T.; Weinert, L. A.; Belkhir, K.; Bierne, N.; Glémin, S.; Galtier, N. Comparative population genomics in animals uncovers the determinants of genetic diversity, Nature, Volume 515 (2014) no. 7526, pp. 261-263 | DOI

[47] Romiguier, J.; Lourenco, J.; Gayral, P.; Faivre, N.; Weinert, L. A.; Ravel, S.; Ballenghien, M.; Cahais, V.; Bernard, A.; Loire, E.; Keller, L.; Galtier, N. Population genomics of eusocial insects: the costs of a vertebrate-like effective population size, Journal of Evolutionary Biology, Volume 27 (2014) no. 3, pp. 593-603 | DOI

[48] Rousselle, M.; Laverré, A.; Figuet, E.; Nabholz, B.; Galtier, N. Influence of Recombination and GC-biased Gene Conversion on the Adaptive and Nonadaptive Substitution Rate in Mammals versus Birds, Molecular Biology and Evolution, Volume 36 (2018) no. 3, pp. 458-471 | DOI

[49] Settepani, V.; Bechsgaard, J.; Bilde, T. Phylogenetic analysis suggests that sociality is associated with reduced effectiveness of selection, Ecology and Evolution, Volume 6 (2016) no. 2, pp. 469-477 | DOI

[50] Sirviö, A.; Johnston, J. S.; Wenseleers, T.; Pamilo, P. A high recombination rate in eusocial Hymenoptera: evidence from the common wasp Vespula vulgaris, BMC Genetics, Volume 12 (2011) no. 1 | DOI

[51] Strobel, H. M.; Hays, S. J.; Moody, K. N.; Blum, M. J.; Heins, D. C. Estimating effective population size for a cestode parasite infecting three-spined sticklebacks, Parasitology, Volume 146 (2019) no. 07, pp. 883-896 | DOI

[52] Tabadkani, S. M.; Nozari, J.; Lihoreau, M. Inbreeding and the evolution of sociality in arthropods, Naturwissenschaften, Volume 99 (2012) no. 10, pp. 779-788 | DOI

[53] Traynor, R. E.; Mayhew, P. J. A comparative study of body size and clutch size across the parasitoid Hymenoptera, Oikos, Volume 109 (2005) no. 2, pp. 305-316 | DOI

[54] Wallberg, A.; Glémin, S.; Webster, M. T. Extreme Recombination Frequencies Shape Genome Variation and Evolution in the Honeybee, Apis mellifera, PLOS Genetics, Volume 11 (2015) no. 4 | DOI

[55] Traynor, R. E.; Mayhew, P. J. Host range in solitary versus gregarious parasitoids: a laboratory experiment, Entomologia Experimentalis et Applicata, Volume 117 (2005) no. 1, pp. 41-49 | DOI

[56] Wang, J.; Santiago, E.; Caballero, A. Prediction and estimation of effective population size, Heredity, Volume 117 (2016) no. 4, pp. 193-206 | DOI

[57] Wcislo, W. T. The Roles of seasonality, host synchrony, and behaviour in the evolutions and distributions of nest parasites in Hymenoptera (Insecta), with special reference to bees (Apoidea), Biological Reviews, Volume 62 (1987) no. 4, pp. 515-542 | DOI

[58] Weinstock, G.; The Honeybee Genome Sequencing Consortium Insights into social insects from the genome of the honeybee Apis mellifera, Nature, Volume 443 (2006) no. 7114, pp. 931-949 | DOI

[59] Warren et al. Functional and Evolutionary Insights from the Genomes of Three Parasitoid Nasonia Species, Science, Volume 327 (2010) no. 5963, pp. 343-348 | DOI

[60] Wertheim, J. O.; Murrell, B.; Smith, M. D.; Kosakovsky Pond, S. L.; Scheffler, K. RELAX: Detecting Relaxed Selection in a Phylogenetic Framework, Molecular Biology and Evolution, Volume 32 (2014) no. 3, pp. 820-832 | DOI

[61] Wilfert, L.; Gadau, J.; Schmid-Hempel, P. Variation in genomic recombination rates among animal taxa and the case of social insects, Heredity, Volume 98 (2007) no. 4, pp. 189-197 | DOI

[62] Wilson, E. O. One Giant Leap: How Insects Achieved Altruism and Colonial Life, BioScience, Volume 58 (2008) no. 1, pp. 17-25 | DOI

[63] Winfree, R. The conservation and restoration of wild bees, Annals of the New York Academy of Sciences, Volume 1195 (2010) no. 1, pp. 169-197 | DOI

[64] Wright, S. Evolution in mendelian populations, Bulletin of Mathematical Biology, Volume 52 (1931) no. 1-2, pp. 241-295 | DOI

[65] Zayed, A.; Packer, L. The population genetics of a solitary oligolectic sweat bee, Lasioglossum (Sphecodogastra) oenotherae (Hymenoptera: Halictidae), Heredity, Volume 99 (2007) no. 4, pp. 397-405 | DOI

[66] Zayed, A.; Packer, L.; Grixti, J. C.; Ruz, L.; Owen, R. E.; Toro, H. Increased genetic differentiation in a specialist versus a generalist bee: implications for conservation, Conservation Genetics, Volume 6 (2006) no. 6, pp. 1017-1026 | DOI

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