The evolutionary history of mariner-like elements in Neotropical
drosophilids
Gabriel Luz Wallau • Aurelie Hua-Van •
Pierre Capy • Elgion L. S. Loreto
Received: 4 May 2010 / Accepted: 17 January 2011 / Published online: 20 February 2011
 Springer Science+Business Media B.V. 2011
Abstract The evolutionary history of mariner-like ele-
ments (MLEs) in 49 mainly Neotropical drosophilid species
is described. So far, the investigations about the distribution
of MLEs were performed mainly using hybridization assays
with the Mos1 element (the first mariner active element
described) in a widely range of drosophilid species and these
sequences were found principally in species that arose in
Afrotropical and Sino-Indian regions. Our analysis in mainly
Neotropical drosophilid species shows that twenty-three
species presented MLEs from three different subfamilies in
their genomes: eighteen species had MLEs from subfamily
mellifera, fifteen from subfamily mauritiana and three from
subfamily irritans. Eleven of these species exhibited ele-
ments from more than one subfamily in their genome. In two
subfamilies, the analyzed coding region was uninterrupted
and contained conserved catalytic motifs. This suggests that
these sequences were probably derived from active ele-
ments. The species with these putative active elements are
Drosophila mediopunctata and D. busckii for the mauritiana
subfamily, and D. paramediostriata for the mellifera sub-
family. The phylogenetic analysis of MLE, shows a complex
evolutionary pattern, exhibiting vertical transfer, stochastic
loss and putative events of horizontal transmission occurring
between different Drosophilidae species, and even those
belonging to more distantly related taxa such as Bactrocera
tryoni (Tephritidae family), Sphyracephala europaea
(Diopsoidea superfamily) and Buenoa sp. (Hemiptera order).
Moreover, our data show that the distribution of MLEs is not
restricted to Afrotropical and Sino-Indian species. Con-
versely, these TEs are also widely distributed in drosophilid
species arisen in the Neotropical region.
Keywords Mariner-like elements  Vertical transfer 
Horizontal transfer  Drosophila  Transposable elements 
Transposon
Introduction
Almost all organisms investigated thus far have a fraction
of their genomes composed by transposable elements
(TEs). Generally, these elements are considered to be
genome parasites. Nevertheless, a continuum from extreme
parasitism to mutualism may exist for the relationship
between TEs and their hosts (Volff 2006). A recognized
characteristic of TEs is that they can move within and
between genomes and can have significant impacts on
their hosts, such as large-scale structural changes, epige-
netic regulatory modifications, production of allelic diver-
sity, creation of new genes, and biological innovations
(Feschotte and Pritham 2007).
Electronic supplementary material The online version of this
article (doi:10.1007/s10709-011-9552-6) contains supplementary
material, which is available to authorized users.
G. L. Wallau  E. L. S. Loreto
Programa de Po´s-Graduac¸a˜o em Biodiversidade Animal, Centro
de Cieˆncias Naturais e Exatas (CCNE), Universidade Federal de
Santa Maria (UFSM), Rua Roraima, 1000, Santa Maria,
RS 97105-900, Brazil
A. Hua-Van  P. Capy
Laboratoire Evolution, Ge´nomes et Spe´ciation, UPR9034,
CNRS, 91198 Gif-sur-Yvette, France
A. Hua-Van  P. Capy
Universite´ Paris-Sud, Orsay Cedex, France
E. L. S. Loreto (&)
Departamento de Biologia-CCNE, Universidade Federal de
Santa Maria, Santa Maria, RS, Brazil
e-mail: elgion.loreto@pq.cnpq.br
123
Genetica (2011) 139:327–338
DOI 10.1007/s10709-011-9552-6

TEs are divided into two main classes depending on
their mechanism of transposition (Finnegan 1989). Class I,
retrotransposons, is composed of elements that use a
transposition mechanism termed ‘copy-and-paste’. This
mechanism uses an RNA intermediate. Class II, termed
transposons, is composed of elements that transpose by a
mechanism called ‘cut-and-paste’ which uses a DNA
intermediate (Wicker et al. 2007).
The mariner family, also called mariner-like elements
(MLEs) or ItmD34D, is one of the best known Class II
element families. It belongs to the order TIR (Terminal
Inverted Repeat) and the superfamily Tc1-Mariner, and is
widespread among metazoans (Auge´-Gouillou et al. 1995;
Garcia-Ferna`ndez et al. 1995; Ren et al. 2006; Robertson
and MacLeod 1993; Silva et al. 2005; Sinzelle et al. 2006).
The broad distribution of MLEs can be explained, in part,
by their incredible ability to move between genomes, a
phenomenon known as Horizontal Transfer (HT) (Brunet
et al. 1999; Maruyama and Hartl 1991b; Laha et al. 2007;
Lampe et al. 2003; Robertson 1997; Robertson and Lampe
1995; Yoshiyama et al. 2001).
MLEs are generally 1.3-kb long and contain inverted
terminal repeats (TIRs) of approximately 28 bp. They
contain a unique ORF (Open Reading Frame) with the
aspartic protein triad DD34D. Due to the great diversity of
MLEs, they are classified into several subfamilies based on
phylogenetic analysis. A general classification of these
elements was recently proposed (Rouault et al. 2009). The
major subfamilies include mauritiana, cecropia, irritans,
mellifera and capitata (Robertson and MacLeod 1993).
However, other minor subfamilies also exist with a more
limited distribution (Robertson et al. 2002; Rouault et al.
2009). Some of these subfamilies encompass autonomous
elements (e.g., the mauritiana subfamily, which includes
the Mos1 element; and the mellifera subfamily, which
includes the Famar1 element), though most of the mariner
elements that have been found to date harbor inactivating
point mutations or frameshifts (Mun˜os-Lopes et al. 2008).
The first mariner element (Dromar) and the first active
copy (Mos1) that were described were isolated from Dro-
sophila mauritiana (Jacobson et al. 1986; Medhora et al.
1988) and belong to the mauritiana subfamily. Subsequent
studies searching for related sequences in Drosophilidae
species were performed, most of which used hybridization
assays with Dromar or Mos1 as probes (Bie´mont and
Cizeron 1999; Brunet et al. 1994, 1999; Capy et al. 1992;
Castro et al. 2006; Germanos et al. 2006; Loreto et al. 1998
and Maruyama and Hartl 1991a). These studies were lar-
gely focused on the Drosophila genus, though some spe-
cies of Zaprinonus, Scaptomyza, Zygothrica, Chymomyza
and Scaptodrosophila were also analyzed. Within the
Drosophila genus, the four Sophophora subgenus species
group (melanogaster, obscura, willistoni and saltans) have
elements of the mauritiana subfamily that are related to the
Mos1 elements. Two other subfamilies have also been
found in the melanogaster group: irritans in D. ananassae
(Robertson and Lampe 1995) and mellifera in several
species of the melanogaster subgroup (Auge´-Gouillou
et al. 1999; Lohe et al. 1995). The elements of these sub-
families exhibit patchy distributions and incongruence
between the phylogeny of the TEs and the phylogeny of
their host species, suggesting that some events of HT have
occurred. Within the Drosophila subgenus, only the Mos1-
like elements from the mauritiana subfamily have been
examined, and these may be present in five species: two
from the virilis group, one from the repleta group and two
from the immigrans group (Bie´mont and Cizeron 1999).
Some Zaprionus and Scaptomyza species also present
elements of the mauritiana subfamily (Brunet et al. 1994,
1999; Maruyama and Hartl 1991a, 1991b).
Based on the distribution of Mos1-like elements in
endemic species of Drosophilidae, Brunet et al. (1994, 1999)
found that Mos1-like elements are mainly present in Asia
and Africa. They proposed two hypotheses to explain this
pattern that are not mutually exclusive: (1) it may result
from the introduction of this element through HT in species
that are endemic to these geographical regions, in which
case the HT could have occurred between Drosophila spe-
cies and/or between Drosophila species and one or several
donor species outside of the Drosophilidae family; (2) it may
correspond to the evolution of the mariner element from an
ancestral copy that was present in the Drosophilidae
ancestor that has been lost from some lineages.
In the study presented here, we have investigated the
evolutionary history of MLEs in 49 Neotropical Droso-
philidae species (including 2 outside the Drosophila genus)
to increase our comprehension of the evolution of these TEs.
Twenty-three of these species have MLEs in their genomes,
and these belong to three different subfamilies: eighteen
species have MLEs from the mellifera subfamily; fifteen
species have MLEs from the mauritiana subfamily; and
three species have MLEs from the irritans subfamily. Three
species have sequences with no stop codons or frameshifts
in the sequenced region: D. mediopunctata and D. busckii
from the mauritiana subfamily and D. paramediostriata for
the mellifera subfamily. Phylogenetic analysis showed
evidence of Vertical Transfer (VT) with stochastic losses
and several putative HT events.
Materials and methods
PCR, cloning and sequencing
Total DNA from 49 Drosophilidae species (Supplementary
Table 1) was prepared according to the method of De
328 Genetica (2011) 139:327–338
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