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Obligate mutualism within a host drives the extreme specialization of a fig wasp genome

Jin-Hua Xiao1, Zhen Yue2, Ling-Yi Jia13, Xin-Hua Yang2, Li-Hua Niu4, Zhuo Wang2, Peng Zhang1, Bao-Fa Sun13, Shun-Min He1, Zi Li13, Tuan-Lin Xiong13, Wen Xin5, Hai-Feng Gu13, Bo Wang13, John H Werren6, Robert W Murphy78, David Wheeler6, Li-Ming Niu9, Guang-Chang Ma9, Ting Tang10, Sheng-Nan Bian4, Ning-Xin Wang4, Chun-Yan Yang4, Nan Wang4, Yue-Guan Fu9, Wen-Zhu Li1, Soojin V Yi11, Xing-Yu Yang11, Qing Zhou2, Chang-Xin Lu2, Chun-Yan Xu3, Li-Juan He2, Li-Li Yu2, Ming Chen2, Yuan Zheng2, Shao-Wei Wang2, Shuang Zhao2, Yan-Hong Li2, Yang-Yang Yu2, Xiao-Ju Qian2, Yue Cai2, Lian-Le Bian2, Shu Zhang2, Jun-Yi Wang2, Ye Yin2, Hui Xiao1, Guan-Hong Wang13, Hui Yu12, Wen-Shan Wu13, James M Cook1415*, Jun Wang2* and Da-Wei Huang1104*

Author Affiliations

1 Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China

2 BGI-Shenzhen, Shenzhen 518083, China

3 University of Chinese Academy of Sciences, Beijing 100039, China

4 College of Plant Protection, Shandong Agricultural University, Tai’an 271018, China

5 Beijing TransGen Biotech Co. Ltd., Beijing 100192, China

6 Biology Department, University of Rochester, Rochester, NY 14627, USA

7 State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China

8 Department of Natural History, Royal Ontario Museum, 100 Queen’s Park, Toronto, Ontario M5S 2C6, Canada

9 Environment and Plant Protection Institute, Chinese Academy of Tropical Agricultural Sciences, Danzhou 571737, China

10 College of Life Science, Hebei University, Baoding 071002, China

11 School of Biology, Georgia Institute of Technology, Atlanta, GA 30332, USA

12 Key Laboratory of Plant Resources Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China

13 College of Life Sciences, Fujian Normal University, Fuzhou 350108, China

14 School of Biological Sciences, University of Reading, Berkshire, Reading RG6 6AH, UK

15 Hawkesbury Institute for the Environment, University of Western Sydney, Locked Bag 1797, Penrith South, DC, NSW 1797, Australia

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Genome Biology 2013, 14:R141  doi:10.1186/gb-2013-14-12-r141

Published: 20 December 2013

Abstract

Background

Fig pollinating wasps form obligate symbioses with their fig hosts. This mutualism arose approximately 75 million years ago. Unlike many other intimate symbioses, which involve vertical transmission of symbionts to host offspring, female fig wasps fly great distances to transfer horizontally between hosts. In contrast, male wasps are wingless and cannot disperse. Symbionts that keep intimate contact with their hosts often show genome reduction, but it is not clear if the wide dispersal of female fig wasps will counteract this general tendency. We sequenced the genome of the fig wasp Ceratosolen solmsi to address this question.

Results

The genome size of the fig wasp C. solmsi is typical of insects, but has undergone dramatic reductions of gene families involved in environmental sensing and detoxification. The streamlined chemosensory ability reflects the overwhelming importance of females finding trees of their only host species, Ficus hispida, during their fleeting adult lives. Despite long-distance dispersal, little need exists for detoxification or environmental protection because fig wasps spend nearly all of their lives inside a largely benign host. Analyses of transcriptomes in females and males at four key life stages reveal that the extreme anatomical sexual dimorphism of fig wasps may result from a strong bias in sex-differential gene expression.

Conclusions

Our comparison of the C. solmsi genome with other insects provides new insights into the evolution of obligate mutualism. The draft genome of the fig wasp, and transcriptomic comparisons between both sexes at four different life stages, provide insights into the molecular basis for the extreme anatomical sexual dimorphism of this species.