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

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.

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.

Figure 2

Extreme morphological dimorphism between female and male fig wasps, C. solmsi. Morphologically, the genders exhibit extreme differences in their compound eyes, wings, antennae, and body color. Scale bar indicates 0.2 mm for each part, except 0.02 mm for male wing.

Figure 3

Phylogenetic relationships and gene-family clusters of 10 species of arthropods. Gray dot (for calibration) represents the divergence time of 307.4 to 238.0 million years ago between Drosophila melanogaster and Apis mellifera based on fossil evidence. Numbers following each species indicate the average numbers of genes per gene family. Single-copy orthologs have only one copy in each species, multicopy orthologs have more than one copy in different species, unique paralogs include the species-specific, other orthologs are unclassified orthologs, and unclustered genes cannot be clustered into known gene families.

Figure 4

Gene family contraction and expansion in 10 arthropod species. Green indicates expansions, red denotes contractions, and blue signposts no obvious change. Compared to the other species, the C. solmsi has the smallest number of expanded gene families.

Figure 5

Heatmap indicating the CPR gene expression through different life stages of fig wasps, C. solmsi. Most of the genes are highly expressed in late pupa stage. The bar indicates expression level ranging from zero to higher. LarvaF: female at larva stage; LarvaM: male at larva stage; Pupae21F: female at early pupa stage (the 21st day after oviposition); Pupae21M: male at early pupa stage (the 21st day after oviposition); Pupae25F: female at late pupa stage (the 25th day after oviposition); Pupae25M: male at late pupa stage (the 25th day after oviposition); AdultF: female at adult stage; AdultM: male at adult stage.

Figure 6

Four main immunity pathways in Drosophila melanogaster and their counterparts in three hymenopteran species. The four main immunity pathways are Toll, immunodeficiency (IMD), c-Jun N-terminal kinase (JNK), and Janus kinase/Signal transducers and activators of transcription (JAK/STAT). The hymenopterans are Apis mellifera, Nasonia vitripennis, and C. solmsi. Gray indicates genes occurring in all four species. Red indicates genes described from D. melanogaster but absent in all hymenopterans. Brown indicates genes absent in the chalcid N. vitripennis and C. solmsi, but present in D. melanogaster and A. mellifera. Blue shows genes absent in C. solmsi only. Green signposts outside infections such as Gram-positive and Gram-negative bacteria, and fungi. Yellow denotes antimicrobial peptides (details in Additional file 1: Table S11).

Figure 7

Gene expression profiles for female and male fig pollinators at four key life stages. (A) Gene expression profiles with highly expressed genes shown in red, moderately expressed genes in black, and low or unexpressed genes in green. (B) Comparisons of the gene numbers with significantly diverged expression between both genders in the four stages of fig wasp (data from abdomen of Drosophila willistoni as control); red columns indicate the percentages of upregulated genes and green columns show the percentages of downregulated genes. Figure 5 provides descriptions of the samples.