In Dichotomius genus, transposable elements (TE) have been related to chromosome remodeling, genomic evolution, and, possibly, to the speciation process. The objective of this study was to verify the interpopulational and interspecific conservation/variation of Tc1-Mariner elements (possibly autonomous) in Dichotomius species, aiming to identify possible contributions in the speciation process of this group. The analysis was performed on four species of Dichotomius, belonging to the Selenocopris subgenus. We verified the presence of the DsPogo_8 and DsTc1_5 elements by PCR and sequencing. We also isolated and sequenced the 28S and 16S rRNA genes aiming at the phylogenetic reconstruction of the analyzed species. Chromosomal mapping of TEs DsTc1_5 and DsPogo_8 was performed by fluorescent in situ hybridization. The results revealed the presence of the elements in the different species analyzed, except for DsTc1_5 in D. (S.) geminatus. These results suggest a vertical inheritance, with the presence of these elements in the common ancestor of these species. In the analyzed species, the nucleotide similarity of DsTc1_5 was higher than that of the 28S and 16S rRNA genes, suggesting the occurrence of horizontal transfer. The phylogenetic tree indicated that the absence of DsTc1_5 in D. (S.) geminatus is related to stochastic loss of this TE. Chromosomal mapping revealed dispersed signals, with predominance in euchromatic regions and wide variation in the chromosomal localization pattern of DsTc1_5 and DsPogo_8, both interpopulational and interspecific. This variation indicates that DsTc1_5 and DsPogo_8 may have contributed to prezygotic and postzygotic isolation, thus contributing to the speciation of these species.

1.
Almojil
D
,
Bourgeois
Y
,
Falis
M
,
Hariyani
I
,
Wilcox
J
,
Boissinot
S
.
The structural, functional and evolutionary impact of transposable elements in eukaryotes
.
Genes
.
2021
;
12
(
6
):
918
.
2.
Amorim
IC
,
Costa
RGC
,
Xavier
C
,
Moura
RC
.
Characterization and chromosomal mapping of the DgmarMITE transposon in populations of Dichotomius (Luederwaldtinia) sericeus species complex (Coleoptera: Scarabaeidae)
.
Genet Mol Biol
.
2018
;
41
(
2
):
419
25
.
3.
Amorim
IC
,
Melo
ES
,
Moura
RC
,
Wallau
GL
.
Diverse mobilome of Dichotomius (Luederwaldtinia) schiffleri (Coleoptera: Scarabaeidae) reveals long-range horizontal transfer events of DNA transposons
.
Mol Genet Genomics
.
2020
;
295
(
6
):
1339
53
.
4.
Amorim
IC
,
Sotero-Caio
CG
,
Costa
RGC
,
Xavier
C
,
de Moura
RC
.
Comprehensive mapping of transposable elements reveals distinct patterns of element accumulation on chromosomes of wild beetles
.
Chromosome Res
.
2021
;
29
(
2
):
203
18
.
5.
Araújo
NP
,
Sena
RS
,
Bonvicino
CR
,
Kuhn
GC
,
Svartman
M
.
SINE-B1 distribution and chromosome rearrangements in the south American Proechimys gr. goeldii (Echimyidae, Rodentia)
.
Cytogenet Genome Res
.
2021
;
161
(
1-2
):
6
13
.
6.
Bargues
N
,
Lerat
E
.
Evolutionary history of LTR-retrotransposons among 20 Drosophila species
.
Mob DNA
.
2017
;
8
(
1
):
7
15
.
7.
Biscotti
MA
,
Olmo
E
,
Heslop-Harrison
JS
.
Repetitive DNA in eukaryotic genomes
.
Chromosome Res
.
2015
;
23
(
3
):
415
20
.
8.
Blumenstiel
JP
.
Birth, school, work, death, and resurrection: the life stages and dynamics of transposable element proliferation
.
Genes
.
2019
;
10
(
5
):
336
.
9.
Bouallègue
M
,
Filée
J
,
Kharrat
I
,
Mezghani-Khemakhem
M
,
Rouault
JD
,
Makni
M
.
Diversity and evolution of mariner-like elements in aphid genomes
.
BMC Genomics
.
2017
;
18
(
1
):
494
.
10.
Bourgeois
Y
,
Boissinot
S
.
On the population dynamics of junk: a review on the population genomics of transposable elements
.
Genes
.
2019
;
10
(
6
):
419
.
11.
Cabral-de-Mello
DC
,
Marec
F
.
Universal fluorescence in situ hybridization (FISH) protocol for mapping repetitive DNAs in insects and other arthropods
.
Mol Genet Genomics
.
2021
;
296
(
3
):
513
26
.
12.
Cabral-de-Mello
DC
,
Moura
RC
,
Martins
C
.
Chromosomal mapping of repetitive DNAs in the beetle Dichotomius geminatus provides the first evidence for an association of 5S rRNA and histone H3 genes in insects, and repetitive DNA similarity between the B chromosome and A complement
.
Heredity
.
2010
;
104
(
4
):
393
400
.
13.
Cabral-de-Mello
DC
,
de Moura
RC
,
de Souza Melo
A
,
Martins
C
.
Evolutionary dynamics of heterochromatin in the genome of Dichotomius beetles based on chromosomal analysis
.
Genetica
.
2011a
;
139
(
3
):
315
25
.
14.
Cabral-de-Mello
DC
,
Moura
RC
,
Martins
C
.
Cytogenetic mapping of rRNAs and histone H3 genes in 14 species of Dichotomius (Coleoptera, Scarabaeidae, Scarabaeinae) beetles
.
Cytogenet Genome Res
.
2011b
;
134
(
2
):
127
35
.
15.
Castresana
J
.
Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis
.
Mol Biol Evol
.
2000
;
17
(
4
):
540
52
.
16.
Chalopin
D
,
Naville
M
,
Plard
F
,
Galiana
D
,
Volff
JN
.
Comparative analysis of transposable elements highlights mobilome diversity and evolution in vertebrates
.
Genome Biol Evol
.
2015
;
7
(
2
):
567
80
.
17.
Dimitri
P
.
Constitutive heterochromatin and transposable elements in Drosophila melanogaster
.
Genetica
.
1997
;
100
(
1-3
):
85
93
.
18.
Gilbert
C
,
Feschotte
C
.
Horizontal acquisition of transposable elements and viral sequences: patterns and consequences
.
Curr Opin Genet Dev
.
2018
;
49
:
15
24
.
19.
Gilbert
C
,
Peccoud
J
,
Cordaux
R
.
Transposable elements and the evolution of insects
.
Annu Rev Entomol
.
2021
;
66
(
1
):
355
72
.
20.
Jurka
J
,
Bao
W
,
Kojima
KK
.
Families of transposable elements, population structure and the origin of species
.
Biol Direct
.
2011
;
6
(
1
):
44
.
21.
Katoh
K
,
Rozewicki
J
,
Yamada
KD
.
MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization
.
Brief Bioinform
.
2019
;
20
(
4
):
1160
6
.
22.
Kent
TV
,
Uzunović
J
,
Wright
SI
.
Coevolution between transposable elements and recombination
.
Philos Trans R Soc Lond B Biol Sci
.
2017
;
372
(
1736
):
20160458
.
23.
Maumus
F
,
Fiston-Lavier
AS
,
Quesneville
H
.
Impact of transposable elements on insect genomes and biology
.
Curr Opin Insect Sci
.
2015
;
7
:
30
6
.
24.
Melo
ES
,
Wallau
GL
.
Mosquito genomes are frequently invaded by transposable elements through horizontal transfer
.
PLoS Genet
.
2020
;
16
(
11
):
e1008946
.
25.
Monaghan
MT
,
Inward
DJ
,
Hunt
T
,
Vogler
AP
.
A molecular phylogenetic analysis of the Scarabaeinae (dung beetles)
.
Mol Phylogenet Evol
.
2007
;
45
(
2
):
674
92
.
26.
Montiel
EE
,
Cabrero
J
,
Camacho
JPM
,
López-León
MD
.
Gypsy, RTE and Mariner transposable elements populate Eyprepocnemis plorans genome
.
Genetica
.
2012
;
140
(
7-9
):
365
74
.
27.
Nunes
RV
,
Vaz-de-Mello
FZ
.
Taxonomic revision of Dichotomius (cephagonus) Luederwaldt 1929 and the taxonomic status of remaining Dichotomius hope 1838 subgenera (Coleoptera: Scarabaeidae: Scarabaeinae: Dichotomiini)
.
J Nat Hist
.
2019
;
53
(
37-38
):
2231
351
.
28.
Oliveira
SG
,
Cabral-de-Mello
DC
,
Moura
RC
,
Martins
C
.
Chromosomal organization and evolutionary history of Mariner transposable elements in Scarabaeinae coleopterans
.
Mol Cytogenet
.
2013
;
6
(
1
):
54
9
.
29.
Palacios-Gimenez
OM
,
Bueno
D
,
Cabral-de-Mello
DC
.
Chromosomal mapping of two Mariner-like elements in the grasshopper Abracris flavolineata (Orthoptera: Acrididae) reveals enrichment in euchromatin
.
Eur J Entomol
.
2014
;
111
(
3
):
329
34
.
30.
Peccoud
J
,
Loiseau
V
,
Cordaux
R
,
Gilbert
C
.
Massive horizontal transfer of transposable elements in insects
.
Proc Natl Acad Sci U S A
.
2017
;
114
(
18
):
4721
6
.
31.
Petersen
M
,
Armisén
D
,
Gibbs
RA
,
Hering
L
,
Khila
A
,
Mayer
G
,
.
Diversity and evolution of the transposable element repertoire in arthropods with particular reference to insects
.
BMC Evol Biol
.
2019
;
19
(
1
):
11
5
.
32.
Ricci
M
,
Peona
V
,
Guichard
E
,
Taccioli
C
,
Boattini
A
.
Transposable elements activity is positively related to rate of speciation in mammals
.
J Mol Evol
.
2018
;
86
(
5
):
303
10
.
33.
Rosolen
LAM
,
Vicari
MR
,
Almeida
MC
.
Accumulation of transposable elements in autosomes and giant sex chromosomes of Omophoita (Chrysomelidae: Alticinae)
.
Cytogenet Genome Res
.
2018
;
156
(
4
):
215
22
.
34.
Sambrook
J
,
Russell
WD
.
Molecular Cloning. A Laboratory Manual
. 3rd ed.
New York
:
Cold Spring Harbor Laboratory Press
;
2001
.
35.
Serrato-Capuchina
A
,
Matute
DR
.
The role of transposable elements in speciation
.
Genes
.
2018
;
9
(
5
):
254
.
36.
Sotero-Caio
CG
,
Platt
RN
,
Suh
A
,
Ray
DA
.
Evolution and diversity of transposable elements in vertebrate genomes
.
Genome Biol Evol
.
2017
;
9
(
1
):
161
77
.
37.
Valois
MC
,
Vaz-de-Mello
FZ
,
Silva
FAB
.
Taxonomic revision of the Dichotomius sericeus (Harold, 1867) species group (Coleoptera: Scarabaeidae: Scarabaeinae)
.
Zootaxa
.
2017
;
4277
(
4
):
503
30
.
38.
Wallau
GL
,
Capy
P
,
Loreto
E
,
Le Rouzic
A
,
Hua-Van
A
.
VHICA, a new method to discriminate between vertical and horizontal transposon transfer: application to the mariner family within Drosophila
.
Mol Biol Evol
.
2016
;
33
(
4
):
1094
109
.
39.
Wallau
GL
,
Vieira
C
,
Loreto
ÉLS
.
Genetic exchange in eukaryotes through horizontal transfer: connected by the mobilome
.
Mob DNA
.
2018
;
9
(
1
):
6
.
40.
Warren
IA
,
Naville
M
,
Chalopin
D
,
Levin
P
,
Berger
CS
,
Galiana
D
.
Evolutionary impact of transposable elements on genomic diversity and lineage-specific innovation in vertebrates
.
Chromosome Res
.
2015
;
23
(
3
):
505
31
.
41.
Wells
JN
,
Feschotte
C
.
A field guide to eukaryotic transposable elements
.
Annu Rev Genet
.
2020
;
54
(
1
):
539
61
.
42.
Xavier
C
,
Cabral-de-Mello
DC
,
de Moura
RC
.
Heterochromatin and molecular characterization of DsmarMITE transposable element in the beetle Dichotomius schiffleri (Coleoptera: Scarabaeidae)
.
Genetica
.
2014
;
142
(
6
):
575
81
.
43.
Yoshida
K
,
Ishikawa
A
,
Toyoda
A
,
Shigenobu
S
,
Fujiyama
A
,
Kitano
J
.
Functional divergence of a heterochromatin‐binding protein during stickleback speciation
.
Mol Ecol
.
2019
;
28
(
6
):
1563
78
.
44.
Yoshitake
Y
,
Inomata
N
,
Sano
M
,
Kato
Y
,
Itoh
M
.
The P element invaded rapidly and caused hybrid dysgenesis in natural populations of Drosophila simulans in Japan
.
Ecol Evol
.
2018
;
8
(
19
):
9590
9
.
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