Cryptic Sex and Many-to-one Coevolution in the Fungus-growing Ant Symbiosis

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2006 Jul 4

PMID 16815974

Citations 44

Authors

Alexander S Mikheyev

Ulrich G Mueller

Patrick Abbot

Affiliations

Soon will be listed here.

Abstract

The fungus-growing ants have long provided a spectacular example of coevolutionary integration. Their ecological success is thought to depend largely on the evolutionary alignment of reproductive interests between ants and fungi after vertical transmission and the ancient suppression of fungal sexuality. In the present study we test these assumptions and provide the first evidence of recombination in attine cultivars, contradicting widely held perceptions of obligate clonality. In addition, we document long-distance horizontal transmission of symbionts between leaf-cutter ant species on mainland Central America and South America and those endemic to Cuba, suggesting both lack of pairwise coevolutionary specificity in ant/cultivar interactions and dispersal of symbionts independent of their ant hosts. The coevolution between leaf-cutters and their fungal symbionts is thus not reciprocally pairwise. Rather, a single widespread and sexual fungal symbiont species is engaged in multiple interactions with divergent ant lineages. Strict fungal clonality and vertical transmission evidently have not played a critical role in the long-term evolutionary or ecological success of this well known mutualism.

Citing Articles

Four New Species of (Boletaceae, Boletales) from Hainan Island, Tropical China.

Deng H, Wang Y, Lei J, Chen Z, Liang Z, Zeng N J Fungi (Basel). 2023; 9(12).

PMID: 38132729 PMC: 10744113. DOI: 10.3390/jof9121128.

, a new tropical bolete from Hainan, southern China.

Jiang S, Mi H, Xie H, Zhang X, Chen Y, Liang Z Mycoscience. 2023; 62(3):205-211.

PMID: 37091322 PMC: 9157763. DOI: 10.47371/mycosci.2021.03.001.

Notes on four species of subgenus (Russulaceae, Russulales) from southern China.

Han Y, Liang Z, Zeng N Front Microbiol. 2023; 14:1140127.

PMID: 37025637 PMC: 10072125. DOI: 10.3389/fmicb.2023.1140127.

Updated taxonomy of Chinese subgenera and (Hydnaceae, Cantharellales): Three new taxa and amended descriptions of one previous species.

Zhang Y, Qin H, Chen Z, Lin W, Liang Z, Jiang S Front Microbiol. 2023; 14:1109831.

PMID: 37007503 PMC: 10064096. DOI: 10.3389/fmicb.2023.1109831.

Microscopic marine invertebrates are reservoirs for cryptic and diverse protists and fungi.

Holt C, Boscaro V, Van Steenkiste N, Herranz M, Mathur V, Irwin N Microbiome. 2022; 10(1):161.

PMID: 36180959 PMC: 9523941. DOI: 10.1186/s40168-022-01363-3.

References

Milne I, Wright F, Rowe G, Marshall D, Husmeier D, McGuire G . TOPALi: software for automatic identification of recombinant sequences within DNA multiple alignments. Bioinformatics. 2004; 20(11):1806-7. DOI: 10.1093/bioinformatics/bth155. View

Mueller , Rehner , Schultz . The evolution of agriculture in ants . Science. 1998; 281(5385):2034-8. DOI: 10.1126/science.281.5385.2034. View

Stanton M . Interacting guilds: moving beyond the pairwise perspective on mutualisms. Am Nat. 2003; 162(4 Suppl):S10-23. DOI: 10.1086/378646. View

Ramesh M, Malik S, Logsdon Jr J . A phylogenomic inventory of meiotic genes; evidence for sex in Giardia and an early eukaryotic origin of meiosis. Curr Biol. 2005; 15(2):185-91. DOI: 10.1016/j.cub.2005.01.003. View

DePriest P . Early molecular investigations of lichen-forming symbionts: 1986-2001*. Annu Rev Microbiol. 2004; 58:273-301. DOI: 10.1146/annurev.micro.58.030603.123730. View

Taylor D, Bruns T . Independent, specialized invasions of ectomycorrhizal mutualism by two nonphotosynthetic orchids. Proc Natl Acad Sci U S A. 1997; 94(9):4510-5. PMC: 20753. DOI: 10.1073/pnas.94.9.4510. View

Mikosch T, Sonnenberg A, van Griensven L . Isolation, characterization, and expression patterns of a DMC1 homolog from the basidiomycete Pleurotus ostreatus. Fungal Genet Biol. 2001; 33(1):59-66. DOI: 10.1006/fgbi.2001.1265. View

Sung P, Krejci L, Van Komen S, Sehorn M . Rad51 recombinase and recombination mediators. J Biol Chem. 2003; 278(44):42729-32. DOI: 10.1074/jbc.R300027200. View

Silva-Pinhati A, Bacci Jr M, Hinkle G, Sogin M, Pagnocca F, Martins V . Low variation in ribosomal DNA and internal transcribed spacers of the symbiotic fungi of leaf-cutting ants (Attini: Formicidae). Braz J Med Biol Res. 2004; 37(10):1463-72. DOI: 10.1590/s0100-879x2004001000004. View

10.

Machado C, Robbins N, Gilbert M, Herre E . Critical review of host specificity and its coevolutionary implications in the fig/fig-wasp mutualism. Proc Natl Acad Sci U S A. 2005; 102 Suppl 1:6558-65. PMC: 1131861. DOI: 10.1073/pnas.0501840102. View

11.

Selosse M . Adding pieces to fungal mosaics. New Phytol. 2021; 149(2):159-162. DOI: 10.1046/j.1469-8137.2001.00047.x. View

12.

Kosakovsky Pond S, Frost S, Muse S . HyPhy: hypothesis testing using phylogenies. Bioinformatics. 2004; 21(5):676-9. DOI: 10.1093/bioinformatics/bti079. View

13.

Hoeksema J, Bruna E . Pursuing the big questions about interspecific mutualism: a review of theoretical approaches. Oecologia. 2017; 125(3):321-330. DOI: 10.1007/s004420000496. View

14.

Paoletti M, Rydholm C, Schwier E, Anderson M, Szakacs G, Lutzoni F . Evidence for sexuality in the opportunistic fungal pathogen Aspergillus fumigatus. Curr Biol. 2005; 15(13):1242-8. DOI: 10.1016/j.cub.2005.05.045. View

15.

Mueller U, Gerardo N . Fungus-farming insects: multiple origins and diverse evolutionary histories. Proc Natl Acad Sci U S A. 2002; 99(24):15247-9. PMC: 137700. DOI: 10.1073/pnas.242594799. View

16.

Aanen D, Eggleton P, Rouland-Lefevre C, Rosendahl S, Boomsma J . The evolution of fungus-growing termites and their mutualistic fungal symbionts. Proc Natl Acad Sci U S A. 2002; 99(23):14887-92. PMC: 137514. DOI: 10.1073/pnas.222313099. View

17.

Currie C, Mueller U, Malloch D . The agricultural pathology of ant fungus gardens. Proc Natl Acad Sci U S A. 1999; 96(14):7998-8002. PMC: 22176. DOI: 10.1073/pnas.96.14.7998. View

18.

West S . Molecular views of recombination proteins and their control. Nat Rev Mol Cell Biol. 2003; 4(6):435-45. DOI: 10.1038/nrm1127. View

19.

Mueller U . Ant versus fungus versus mutualism: ant-cultivar conflict and the deconstruction of the attine ant-fungus symbiosis. Am Nat. 2008; 160 Suppl 4:S67-98. DOI: 10.1086/342084. View

20.

Bot A, Rehner S, Boomsma J . Partial incompatibility between ants and symbiotic fungi in two sympatric species of Acromyrmex leaf-cutting ants. Evolution. 2002; 55(10):1980-91. DOI: 10.1111/j.0014-3820.2001.tb01315.x. View