Genome‐wide sequence data suggest the possibility of pollinator sharing by host shift in dioecious figs (Moraceae, Ficus)

Abstract

The obligate mutualism of figs and fig-pollinating wasps has been one of the classic models used for testing theories of co-evolution and cospeciation due to the high species-specificity of these relationships. To investigate the species-specificity between figs and fig pollinators and to further understand the speciation process in obligate mutualisms, we examined the genetic differentiation and phylogenetic relationships of four closely related fig-pollinating wasp species (Blastophaga nipponica, Blastophaga taiwanensis, Blastophaga tannoensis and Blastophaga yeni) in Japan and Taiwan using genome-wide sequence data, including mitochondrial DNA sequences. In addition, population structure was analysed for the fig wasps and their host species using microsatellite data. The results suggest that the three Taiwanese fig wasp species are a single panmictic population that pollinates three dioecious fig species, which are sympatrically distributed, have large differences in morphology and ecology and are also genetically differentiated. Our results illustrate the first case of pollinator sharing by host shift in the subgenus Ficus. On the other hand, there are strict genetic codivergences between allopatric populations of the two host-pollinator pairs. The possible processes that produce these pollinator-sharing events are discussed based on the level and pattern of genetic differentiation in these figs and fig wasps.

Sky islands as foci for divergence of fig trees and their pollinators in southwest China

“…An increasing number of fig tree species are known to be pollinated by two or more species of fig wasps, a feature that contrasts with the other well‐known nursery pollination system involving yucca moths and their yucca hosts (Smith, Drummond, Godsoe, Yoder, & Pellmyr, ; Yang et al, ; Yu, Tian, et al, ). Fig wasp colonization events followed by host switches have been reported among Ficus species (Wachi, Kusumi, Tzeng, & Su, ), but the northern, montane distribution of F. tikoua means that there is little range overlap with other Ficus species and fewer opportunities for host switching than would be the case for a tropical species. It is more common for fig wasps that share a host Ficus to be “cryptic” species that are difficult to tell apart morphologically (Chen et al, ; Darwell, Al‐Beidh, & Cook, ; Darwell & Cook, ; Rodriguez et al, ; Segar et al, ; Wachi et al, ; Wang, Cannon, & Chen, ; Yu, Tian, et al, ).…”

“…Fig wasp colonization events followed by host switches have been reported among Ficus species (Wachi, Kusumi, Tzeng, & Su, ), but the northern, montane distribution of F. tikoua means that there is little range overlap with other Ficus species and fewer opportunities for host switching than would be the case for a tropical species. It is more common for fig wasps that share a host Ficus to be “cryptic” species that are difficult to tell apart morphologically (Chen et al, ; Darwell, Al‐Beidh, & Cook, ; Darwell & Cook, ; Rodriguez et al, ; Segar et al, ; Wachi et al, ; Wang, Cannon, & Chen, ; Yu, Tian, et al, ). They are typically sister species that have diverged during the history of their association with the plant (Souto‐Vilaros et al, ; Wang et al, ; Yang et al, ; Yu, Tian, et al, ).…”

Faster speciation of fig‐wasps than their host figs leads to decoupled speciation dynamics: Snapshots across the speciation continuum

“…We suggest that both temperature gradients and cloud cover will pose problems to dispersing fig wasps, indeed the largest genetic turnover is found between 1,200 m and 2,200 m. Horizontal distances are generally small between our study sites (<10 km) and isolation by distance is not found in F. arfakensis across larger distances (~80 km; Segar et al, ). Due to their short life‐span, assortative mating within the fig before emergence, and weak dispersal abilities, specifically for below‐canopy pollinators (Dev et al, ; Wachi et al, ), fig wasps seem to speciate along their host's range, perhaps aided by a resistance to Allee effects and genetic incompatibilities driven by Wolbachia (Yu et al, ). This structuring within wasps may eventually restrict pollen movement, promoting fig population structure and ultimately, host fig speciation (Cook & Segar, ).…”

“…Even though fig wasps are generally highly mobile dispersers, relying on passive dispersal by wind (Ahmed, Compton, Butlin, & Gilmartin, ; Kobmoo, Hossaert‐Mckey, Rasplus, & Kjellberg, ; Liu, Compton, Peng, Zhang, & Chen, ), their mobility, and thereby the gene flow between their host plants, may sometimes be impaired. For instance, fig wasps associated with dioecious and under‐canopy fig species have limited flight ability (Venkateswaran, Kumble, & Borges, ), which is further compounded by the fact that dioecious fig trees tend to cluster into dense local populations (Dev, Kjellberg, Hossaert‐Mckey, & Borges, ; Wachi, Kusumi, Tzeng, & Su, ). In contrast, wide‐ranging monoecious species have little genetic structure over much of their ranges (Bain et al, ) and their pollinating wasps have been shown to be good dispersers (Venkateswaran et al, ).…”

The Ficus erecta genome to identify the Ceratocystis canker resistance gene for breeding programs in common fig (F. carica)

“…The F. erecta genome characterized in this study provided insights into Ceratocystis canker resistance breeding strategies as well as identified responsible candidates for the resistance and sex determination genes. The genome resources will also be valuable for identifying the mechanisms underlying F. erecta resistance to other diseases or to pests such as nematodes (Hosomi, 1993) and may also contribute to our understanding of genome coevolution between F. erecta and the fig wasp ( Blastophaga nipponica ) (Wachi et al, 2016).…”