Affiliations
1Institute of Entomology, College of Life Sciences, Nankai University, Tianjin 300071, China
2Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
*Correspondence to Da-Wei Huang (huangdw@ioz.ac.cn) and Jin-Hua Xiao (xiaojh@nankai.edu.cn)
Abstract
The co-evolution of fig wasps with fig trees provide an excellent model for studying ecological systems and adaptive evolution. Transposable elements (TEs), as an important component of the genomes, are the powerful driver for environmental adaptation of the organisms. Here, the TEs in the genomes of six pollinator and five non-pollinator species were analyzed in the characteristics of composition, historical burst patterns, and their possible effects on the functions of conjunctive genes. Compared with pollinators, non-pollinators’ TEs showed a significant burst state with more types, longer lengths, and higher contents in the genomes, which might be related to their different evolutionary and life histories, as well as their different sensitivity to environmental changes. However, we identified a common TE burst peak period of 32-34 Mya in both groups, highly consistent with the glacial epoch of Eocene-Oligocene transition in geological history. Further functional enrichment analysis of the genes within 1 Kb near the insertion positions of TEs in the four geological periods representing the major continental ice sheet growth or decay was demonstrated, and the results showed that large amount of TEs were inserted near genes related to the environmental information processing, especially the Circadian entrainment pathway. These TEs might act ascis -regulatory modules to regulate the conjunctive genes in response to geo-climate changes. These results revealed the molecular basis of the fig wasp’s response to changes in the syconia microenvironment and paleoclimate macroenvironment from the perspective of genomic TEs.
Keywords:transposable elements, fig wasp, adaptive evolution, geo-climate,cis -regulatory modules
Introduction
Fig wasps (Hymenoptera: Chalcidoidea) coevolved with figs (Moraceae, Ficus ) are model insects for studying ecological issues and adaptive evolution (Cook and Rasplus 2003). Based on whether they can pollinate, fig wasps are classified into pollinators and non-pollinators (Marussich and Machado 2007). Pollinators feed on the floret ovaries of the syconia of figs. The female pollinators have wings, while the males are wingless. The processes of embryonic development, maturation, mating, and female pollination and oviposition of pollinators are all completed inside the enclosed syconia, and the only step out of the syconia in their life histories is that the mated females fly out to look for other figs in the female phase. Once suitable figs are found, female pollinators immediately enter the syconia to lay eggs and pollinate the florets. However, the life histories of non-pollinators related to figs are relatively complicated. According to diets, they can be classified into gallers, seed predators, kleptoparasites, and parasitoids. Although the developmental process must be completed in the syconia, some winged males will fly out to mate, and the oviposition behaviors of females are mostly completed by penetrating through the sycomium wall from the outside with their long ovipositors (Borges 2015). Previous phylogenetic analyses have suggested that the symbiosis of pollinators and non-pollinators with figs have been evolved at least twice independently (Rasplus, Kerdelhue et al. 1998, Peters, Niehuis et al. 2018). Our previously reported genomic data showed that, compared with non-pollinators, pollinators have dramatically reduced gene families involved in environmental sensing and detoxification and have lost several genes in response to environmental stress and immune activation; many more genes were subject to relaxed selection (Xiao, Wei et al. 2021). Obviously, although both are related to figs, pollinators and non-pollinators have different life and evolutionary histories, and each of them has thus shown diverse adaptation characteristics in the aspect of functional gene evolution.
The life history of fig wasps is closely connected with the enclosed fig fruits, which forms an inseparable relationship between the fates of fig wasps and their host fig trees. Fig trees are typical tropical and subtropical plants, and the distribution is expected to be strongly structured by climate for the sensitivity to geo-climatic changes (Hawkins, Field et al. 2003). Molecular clock data has shown that the origin of figs is ca 75 Mya (Cruaud, Ronsted et al. 2012). Since 65 My, the Cenozoic global climate has undergone a major and complex change, and four intervals of the time-series, including 0.0 to 4.0, 12.5 to 16.5, 20.5 to 24.5, and 31.0 to 35.0 Mya, represent the periods of major continental ice-sheet growth or decay (Zachos, Pagani et al. 2001). The most famous climate anomalies are the abnormally high temperature event at ~55 Mya, and the sudden temperature drop caused by the two glaciation events at ~34 Mya (Ivany, Patterson et al. 2000) and ~23 Mya (Zachos, Shackleton et al. 2001). Rapid climate change is likely to cause a range of selection pressure on organisms on earth, and evolutionary adaptation can be an important way for the latter to surmount rapid climate changes (Hoffmann and Sgro 2011). Since the responses of fig trees to paleoclimate changes have hardly been considered, due to the lack of good palynological records, we expect to find evidence that the evolution of these small insects closely related to the figs is affected by drastic paleoclimate anomalies, from the genomic perspective.
As an important component of the genome, TEs are potent facilitators of genome rapid adaptive evolution (Legrand, Caron et al. 2019). For an organism, the rapid increase in the number and the expansion in the types of TEs are part of the main reasons for genome size growth. Therefore, the content of TEs in different species varies greatly, and it is generally positively correlated with genome size (Shao, Han et al. 2019). According to the “TE-Thrust” hypothesis, a suitable repertoire of TEs can increase the adaptability of species to environmental or ecological changes. Otherwise, the population may undergo a series of evolutionary phenomena, such as stasis, becoming “living fossils”, or even becoming extinct (Oliver and Greene 2011). TE bursts are the most direct cause of the increase of TE contents. In evolutionary history, the highest peak of TE contents in a species is the major burst peak, implying the largest TE component change reserved in the genome related to environmental adaptation (Belyayev 2014, Schrader and Schmitz 2019). TE bursts induced by stress may be the genomic response to rapid external environment changes in natural populations. For example, the genome of the invasive ant Cardiocondyla obscuriorpossesses a quickly evolving accumulation of TEs (TE islands) distributed in the same region as the olfactory receptor gene, which is speculated to be related to the adaptive radiation (Schrader, Kim et al. 2014). In the genome, TEs will affect their neighboring genes. For example, new insertion or excision of TEs can affect the transcription of genes, and TEs evolved into regulatory sequences, such as cis -regulatory elements, which further affect gene expression (Oliver and Greene 2011, van’t Hof, Campagne et al. 2016).
The different life and evolutionary histories of pollinators and non-pollinators imply different adaptation processes, but the evolutionary mechanism of TEs in these processes is still unclear. In this study, we analyze the composition differences and the characteristics of the burst patterns of TEs in 11 fig wasp species, mainly focusing on the relationship of TE bursts with paleoclimate changes and its molecular basis, aming to uncover the adaptative changes of fig wasps to the syconia microenvironment and the geo-climatic macroenvironment from the perspective of evolution of TEs.
Materials and Methods
Data collection
The detailed information of the 11 fig wasps were listed in supplementary Table S1, with all genomes used in this study downloaded from NCBI. The genome accession IDs of the other five species were GCF_009193385.2 (N. vitripennis ), GCF_003254395.2 (A. mellifera ), GCF_000001215.4 (D. melanogaster ), GCF_005508785.1 (A. pisum ), and GCA_000187875.1 (D. pulex ).