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 ).