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

Xiao et al. Genome Biology Obligate mutualism within a host drives the extreme specialization of a fig wasp genome Jin-Hua Xiao 1 Zhen Yue 0 Ling-Yi Jia 1 Xin-Hua Yang 0 Li-Hua Niu Zhuo Wang 0 Peng Zhang 1 Bao-Fa Sun 1 Shun-Min He 1 Zi Li 1 Tuan-Lin Xiong 1 Wen Xin Hai-Feng Gu 1 Bo Wang 1 John H Werren Robert W Murphy David Wheeler Li-Ming Niu Guang-Chang Ma Ting Tang Sheng-Nan Bian Ning-Xin Wang Chun-Yan Yang Nan Wang Yue-Guan Fu Wen-Zhu Li 1 Soojin V Yi Xing-Yu Yang Qing Zhou 0 Chang-Xin Lu 0 Chun-Yan Xu Li-Juan He 0 Li-Li Yu 0 Ming Chen 0 Yuan Zheng 0 Shao-Wei Wang 0 Shuang Zhao 0 Yan-Hong Li 0 Yang-Yang Yu 0 Xiao-Ju Qian 0 Yue Cai 0 Lian-Le Bian 0 Shu Zhang 0 Jun-Yi Wang 0 Ye Yin 0 Hui Xiao 1 Guan-Hong Wang 1 Hui Yu Wen-Shan Wu James M Cook 2 Jun Wang 0 Da-Wei Huang 1 0 BGI-Shenzhen , Shenzhen 518083 , China 1 Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences , Beijing 100101 , China 2 School of Biological Sciences, University of Reading , Berkshire, Reading RG6 6AH , UK 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. - Background In symbiosis, different species live together intimately. Symbiosis is responsible for several major transitions in evolution, including the origin of eukaryotes, and it underpins key ecosystem functions like nitrogen fixation and pollination [1]. In this system, a large species (host) usually interacts with a smaller one (symbiont), which may live inside it as an endosymbiont. Interactions can be antagonistic, when the symbiont harms the host, such as for parasites and most plant-herbivore interactions [2], or mutualistic, where host and symbiont both benefit from the association and their evolutionary interests are more closely aligned [1,3]. Obligate herbivore-plant mutualisms are relatively uncommon, but the fig pollinating wasp-fig mutualism is an ancient and stable association that originated about 75 million years ago [4]. Typically, endosymbionts are host-specific and show specialized adaptations to life inside their hosts [5,6]. For example, parasites often exhibit a series of morphological reductions. Symbionts may also tend towards gene loss and genome reduction [7]. For example, parasites like tapeworms [8] and the mutualistic bacterium Buchnera [9,10] have smaller genomes than their free-living relatives. Many endosymbionts spend most or all of their lives in the host [5,6] and are vertically transmitted from one host generation to the next, often through eggs or propagules [9-11]. Even when an endosymbiont has a free-living stage, it is often quiescent (for example, tapeworm eggs); transmission to other hosts occurs via host contact or through food or water. Consequently, most obligate endosymbionts, benign or parasitic, live most of their lives in somewhat simplified, relatively predictable environments, allowing selective reduction of their anatomies and genomes [5,6]. Fig-pollinating wasps (Agaonidae: Hymenoptera), hereafter referred to as fig wasps or fig pollinators for brevity, have an obligate, pollinating mutualism with fig trees (Ficus: Moracae) [12,13]. Therefore, unlike most other insect herbivores (for example, Tribolium beetles, pea aphids, diamondback moths), fig wasps are highly mutualistic with the plants upon which they feed. This is one of the most dramatic and ancient examples of an obligatory herbivore-plant mutualism known. Males spend their entire lives inside figs, but females have a brief (1 to 2 day) free-living adult stage that is crucial because these tiny wasps (2 to 5 mm long) achieve record feats of dispersal to lay eggs in trees up to 160 km away [14,15] (Figure 1). Figure 1 Life cycle of fig-fig pollinator mutualism on Ficus hispida. Development of the fig pollinator C. solmsi is mapped onto the developmental stages of the fig fruit. The fig is dioecious; female trees produce fig seeds only, and male trees produce fig wasps only. Selection on males favors anatomical and genomic reductions, but selection on females may oppose this. The need of female fig wasps to disperse great distances and precisely locate and enter host figs requires impressive environmental sensing and locomotor abilities. Thus, sexdifferential selection results in extreme anatomical sexual dimorphism (Figure 2). Female fig wasps resemble other related wasps, although their narrow heads and detachable antennae are key adaptations for entering figs. In contrast, being wingless, de-pigmented, having reduced antennae and eyes [12,13], males show a series of morphological reductions befitting obligate endosymbionts. Ceratosolen solmsi is the obligate pollinating wasp of Ficus hispida, and it has the lifestyle and morphological characters typical of fig pollinators (Figures 1 and 2). We investigate how the longstanding mutualism and largely endosymbiotic lifestyle have shaped the genome of this herbivorous insect by deciphering the draft genome, as well as exploring life-staged transcriptomic differences between both sexes. We also test whether this largely endosymbiotic lifestyle has led to the endosymbiont signature of genome reduction, or if a life cycle with dispersive females prevents this from happening. In the latter case, we predict that male morphological reduction largely reflects reduced (...truncated)