Trajectory and genomic determinants of fungal-pathogen speciation and host adaptation

Author

1. Xiao Hua,1, 
2. Guohua Xiaoa,1,2, 
3. Peng Zhenga, 
4. Yanfang Shanga, 
5. Yao Sub, 
6. Xinyu Zhangb, 
7. Xingzhong Liub,
8. Shuai Zhana, 
9. Raymond J. St. Legerc, and 
10. Chengshu Wanga,3

Author Affiliations

1. aKey Laboratory of Insect Developmental and Evolutionary Biology, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China;
2. bState Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China; and
3. cDepartment of Entomology, University of Maryland, College Park, MD 20742

1. Edited by Jay C. Dunlap, Geisel School of Medicine at Dartmouth, Hanover, NH, and approved October 3, 2014 (received for review July 4, 2014)

Significance

Fossil records have provided compelling evidence for evolution, but lack of existing transitional species has hindered our understanding of speciation at the molecular level. Genomic analyses of seven Metarhizium species revealed a directional speciation continuum from specialists with narrow host ranges to transitional species and then to generalists that paralleled insect evolution. This diversification was coupled with a complex interplay between an array of genomic features that worked together to drive fungal speciation at an accelerating rate and provided a roadmap for identifying variation underlying adaptation and speciation. In particular, specialization was associated with retention of sexuality and rapid evolution of existing protein sequences whereas generalization was associated with loss of sexuality and protein-family expansion.

Abstract

Much remains unknown regarding speciation. Host–pathogen interactions are a major driving force for diversification, but the genomic basis for speciation and host shifting remains unclear. The fungal genus Metarhizium contains species ranging from specialists with very narrow host ranges to generalists that attack a wide range of insects. By genomic analyses of seven species, we demonstrated that generalists evolved from specialists via transitional species with intermediate host ranges and that this shift paralleled insect evolution. We found that specialization was associated with retention of sexuality and rapid evolution of existing protein sequences whereas generalization was associated with protein-family expansion, loss of genome-defense mechanisms, genome restructuring, horizontal gene transfer, and positive selection that accelerated after reinforcement of reproductive isolation. These results advance understanding of speciation and genomic signatures that underlie pathogen adaptation to hosts.

For further details logon website :
http://www.pnas.org/content/111/47/16796.short