Relaxed Selection Underlies Genome Erosion in Socially Parasitic Ant Species

Overview

Journal Nat Commun

Specialty Biology

Date 2021 May 19

PMID 34006882

Citations 17

Authors

Lukas Schrader

Hailin Pan

Martin Bollazzi

Morten Schiott

Fredrick J Larabee

Xupeng Bi

Yuan Deng

Guojie Zhang

Jacobus J Boomsma

Christian Rabeling

Affiliations

Soon will be listed here.

Abstract

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.

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References

Nygaard S, Hu H, Li C, Schiott M, Chen Z, Yang Z . Reciprocal genomic evolution in the ant-fungus agricultural symbiosis. Nat Commun. 2016; 7:12233. PMC: 4961791. DOI: 10.1038/ncomms12233. View

Zhang G, Cowled C, Shi Z, Huang Z, Bishop-Lilly K, Fang X . Comparative analysis of bat genomes provides insight into the evolution of flight and immunity. Science. 2012; 339(6118):456-60. PMC: 8782153. DOI: 10.1126/science.1230835. View

Zhou X, Rokas A, Berger S, Liebig J, Ray A, Zwiebel L . Chemoreceptor Evolution in Hymenoptera and Its Implications for the Evolution of Eusociality. Genome Biol Evol. 2015; 7(8):2407-16. PMC: 4558866. DOI: 10.1093/gbe/evv149. View

Niemiller M, Fitzpatrick B, Shah P, Schmitz L, Near T . Evidence for repeated loss of selective constraint in rhodopsin of amblyopsid cavefishes (Teleostei: Amblyopsidae). Evolution. 2013; 67(3):732-48. DOI: 10.1111/j.1558-5646.2012.01822.x. View

Chen X, Fang D, Wu C, Liu B, Liu Y, Sahu S . Comparative Plastome Analysis of Root- and Stem-Feeding Parasites of Santalales Untangle the Footprints of Feeding Mode and Lifestyle Transitions. Genome Biol Evol. 2019; 12(1):3663-3676. PMC: 6953812. DOI: 10.1093/gbe/evz271. View

Brandt M, Foitzik S, Fischer-Blass B, Heinze J . The coevolutionary dynamics of obligate ant social parasite systems--between prudence and antagonism. Biol Rev Camb Philos Soc. 2005; 80(2):251-67. DOI: 10.1017/s1464793104006669. View

Vogel A, Schwacke R, Denton A, Usadel B, Hollmann J, Fischer K . Footprints of parasitism in the genome of the parasitic flowering plant Cuscuta campestris. Nat Commun. 2018; 9(1):2515. PMC: 6023873. DOI: 10.1038/s41467-018-04344-z. View

Wernegreen J . Endosymbiont evolution: predictions from theory and surprises from genomes. Ann N Y Acad Sci. 2015; 1360:16-35. PMC: 4600008. DOI: 10.1111/nyas.12740. View

Schrader L, Pan H, Bollazzi M, Schiott M, Larabee F, Bi X . Relaxed selection underlies genome erosion in socially parasitic ant species. Nat Commun. 2021; 12(1):2918. PMC: 8131649. DOI: 10.1038/s41467-021-23178-w. View

10.

Moran N . Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc Natl Acad Sci U S A. 1996; 93(7):2873-8. PMC: 39726. DOI: 10.1073/pnas.93.7.2873. View

11.

Gruter C, Jongepier E, Foitzik S . Insect societies fight back: the evolution of defensive traits against social parasites. Philos Trans R Soc Lond B Biol Sci. 2018; 373(1751). PMC: 6000133. DOI: 10.1098/rstb.2017.0200. View

12.

Li H, Sosa-Calvo J, Horn H, Pupo M, Clardy J, Rabeling C . Convergent evolution of complex structures for ant-bacterial defensive symbiosis in fungus-farming ants. Proc Natl Acad Sci U S A. 2018; 115(42):10720-10725. PMC: 6196509. DOI: 10.1073/pnas.1809332115. View

13.

Jones J, Wallberg A, Christmas M, Kapheim K, Webster M . Extreme Differences in Recombination Rate between the Genomes of a Solitary and a Social Bee. Mol Biol Evol. 2019; 36(10):2277-2291. DOI: 10.1093/molbev/msz130. View

14.

Sasaki M, Lange J, Keeney S . Genome destabilization by homologous recombination in the germ line. Nat Rev Mol Cell Biol. 2010; 11(3):182-95. PMC: 3073813. DOI: 10.1038/nrm2849. View

15.

Chang E, Neuhof M, Rubinstein N, Diamant A, Philippe H, Huchon D . Genomic insights into the evolutionary origin of Myxozoa within Cnidaria. Proc Natl Acad Sci U S A. 2015; 112(48):14912-7. PMC: 4672818. DOI: 10.1073/pnas.1511468112. View

16.

Savolainen R, Vepsalainen K . Sympatric speciation through intraspecific social parasitism. Proc Natl Acad Sci U S A. 2003; 100(12):7169-74. PMC: 165848. DOI: 10.1073/pnas.1036825100. View

17.

Tsai I, Zarowiecki M, Holroyd N, Garciarrubio A, Sanchez-Flores A, Brooks K . The genomes of four tapeworm species reveal adaptations to parasitism. Nature. 2013; 496(7443):57-63. PMC: 3964345. DOI: 10.1038/nature12031. View

18.

McCutcheon J, Moran N . Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol. 2011; 10(1):13-26. DOI: 10.1038/nrmicro2670. View

19.

Yin W, Wang Z, Li Q, Lian J, Zhou Y, Lu B . Evolutionary trajectories of snake genes and genomes revealed by comparative analyses of five-pacer viper. Nat Commun. 2016; 7:13107. PMC: 5059746. DOI: 10.1038/ncomms13107. View

20.

Helmkampf M, Cash E, Gadau J . Evolution of the insect desaturase gene family with an emphasis on social Hymenoptera. Mol Biol Evol. 2014; 32(2):456-71. PMC: 4298175. DOI: 10.1093/molbev/msu315. View