Introduction
Bumblebees are very important pollinators of both crops and native
plants and consist of 250 species worldwide (Michener, 2000; Williams,
1998). After the improvements in mass rearing methods, bumblebees are
increasingly used for pollination of crops, primarily for tomato
pollination in greenhouses (Velthuis & van Doorn, 2006). It is
estimated that more than two million commercially reared bumblebee
colonies are used for the pollination globally each year (Lecocq,
Coppee, Michez, Brasero , Rasplus, Valterova, & Rasmont, 2016).
Currently, five species of bumblebees are reared commercially. The main
species is the buff-tailed bumblebee, Bombus terrestris L. It is
naturally distributed mainly in Europe, in coastal North Africa, and in
West and Central Asia. Since the late 1980s, commercially rearedB. terrestris colonies have been transported to many countries,
in every continent except Australia and North America (Rasmont, Coppee,
Michez, & Meullemeester, 2008; Velthuis & van Doorn, 2006). Shortly
after commercial introduction widely beyond its natural area of
distribution, it was recognized that B. terrestris is invasive
and may disturb local ecosystems including; competition for nest sites
and food resources with local bee fauna, genetic contamination of localBombus spp ., and spread of parasites and pathogens (Dafni, Kevan,
Gross, & Goka, 2010).
B. terrestris comprises nine recognized subspecies which differ
in morphology (particularly the pattern of coat colour), genetic,
behavior, colony size, etc. and inhabit separate geographic regions,
sometimes overlapping. Although many subspecies of B. terrestriswere used in the early years of commercial rearing, today Bombus
terrestris dalmatinus has become the main commercialized subspecies due
to the suitable characteristics for mass rearing such as the large size
of workers and high success rate of colonies. Bombus terrestris
terrestris is also currently produced by some companies. Commercial
produced colonies probably originate from stocks collected from the
Turkey, Greece and Balkan Peninsula (B. t. dalmatinus )
and the northern Europe (B. t. terrestris ) (Lecocq, Rasmont,
Harpke, & Schweiger,
2016;
Rasmont, Coppee, Michez, & Meullemeester, 2008; Velthuis & van Doorn,
2006).
There are many characteristics which may contribute to making B.
terrestris invasive including; high migration ability, early seasonal
emergence, high adaptability under adverse climatic conditions in
various habitats, generalist or polylectic foraging strategies,
thermoregulatory metabolism that allows it to be active at low
temperatures, high reproductive abilities, being able to regulate life
cycle in a year with or without hibernation or aestivation (Dafni,
Kevan, Gross, & Goka, 2010). Additionally, commercial B.
terrestris colonies produce more gynes (queens) and are better
competitors than the local conspecific populations. (Gosterit & Gurel,
2005; Ings, Ward, & Chittka, 2006). A single commercial B.
terrestris colony is capable of producing more than a hundred gynes
(new queens) and males which potentially could escape from greenhouses.
Therefore, commercially produced B. terrestris populations are
able to establish and spread into the wild of both native and non-native
regions. In fact, commercial greenhouse B. terrestris populations
have become established outside its native range in many countries such
as, New Zealand, Tasmania, Japan, Chile and Argentina (Buttermore, 1997;
Goka, 2010; Montalva, Dudley, Arroyo, Retamales, & Abrahamovich, 2011;
Morales, Arbetman, Cameron, & Aizen, 2013). Within its native range,
the large-scale use of B. terrestris in greenhouse also raises
concerns about the genetic introgression between commercial and nativeB. terrestris populations which include recognized subspecies or
distinct populations. For instance, Kraus, Szentgyorgyi, Rozej, Rhode,
Moron, Woyciechowski, & Moritz, (2011) in Poland found strong genetic
introgression from the sampled greenhouse populations into the adjacent
populations also found that more distant populations were much less
affected by genetic introgression from the greenhouses. Goulson (2010)
suggested that since the beginning of the bumblebee trade in the 1980s,Bombus terrestris audax which is endemic to Britain and Ireland
may have already merged with commercial produced B. t. dalmatinusand B. t. terrestris through introgression resulting in a single
population. Recently potential hybrids between managed B. t.
terrestris /dalmatinus and Bombus terrestris lusitanicus (endemic
in Iberian Peninsula) have been reported by Cejas, Ornosa,
Munoz, & De la Rua, (2018) and Seabra et al. (2019).
B. t. dalmatinus is the only native B. terrestrissubspecies that is found in Turkey. This subspecies of bumble bees are
the most widespread and live at different altitudes and habitats in the
country. Therefore, there are probably several ecotypes of this
subspecies such as aestivated and hibernated populations, each adapted
to specific ecological conditions; from the Mediterranean coastal areas
to the high mountain conditions of the central Anatolian region. (Gurel,
Gosterit, & Eren, 2008; Ozbek, 1997; Yeninar, Duchateau, Kaftanoglu,
&Velthuis, 2000). On the other hand, commercially produced B.
terrestris colonies began to use as a tomatoes pollinator in 1997. The
number of commercial colonies used has increased enormously year by year
and annually reached to almost 300 000 colonies in 2018 in Turkey.
Because of the lack of regulations with respect to introduction of non -
native B. terrestris subspecies, the movement of
commercial B. terrestris colonies has largely been without risk
assessment and poses a significant disease transmission and
hybridization risk. The consequences of commercialization on wild
populations, the extent of their spread, the degree of genetic
introgression into wild populations are not well understood. Therefore,
in this study we sampled B. terrestris from greenhouses
(belonging to all local and global companies), within the 5 km areas
surrounding the greenhouses and more distant native populations in the
Mediterranean region to determine the genetic structure of native and
commercial B. terrestris populations and to better understand
genetic introgression of commercial greenhouse B. terrestrispopulations into the native B. t. dalmatinus populations using
twenty microsatellite markers and two mitochondrial genes (COIand cyt b ).