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Biological Journal of the Linnean Society, 2014, 111, 699718. With 4 figures
REVIEW ARTICLE
An emerging example of tritrophic coevolution between
flies (Diptera: Fergusoninidae) and nematodes
(Nematoda: Neotylenchidae) on Myrtaceae host plants
LEIGH A. NELSON1, KERRIE A. DAVIES2*, SONJA J. SCHEFFER3, GARY S. TAYLOR4,
MATTHEW F. PURCELL5, ROBIN M. GIBLIN-DAVIS6, ANDREW H. THORNHILL7 and
DAVID K. YEATES1
1
CSIRO Ecosystem Sciences, Clunies Ross Street, Acton, ACT 2601, Australia
Australian Centre for Evolutionary Biology and Biodiversity, and School of Agriculture, Food and
Wine, The University of Adelaide, Waite Campus, PMB 1, Glen Osmond, SA 5064, Australia
3
Systematic Entomology Lab, USDA-ARS, 10300 Baltimore Av., Beltsville, MD 20705, USA
4
Australian Centre for Evolutionary Biology and Biodiversity, and School of Earth and
Environmental Sciences, The University of Adelaide, North Terrace, Adelaide, SA 5005, Australia
5
CSIRO Ecosystem Sciences/USDA ARS Australian Biological Control Laboratory, GPO Box 2583,
Brisbane, Qld 4001, Australia
6
Fort Lauderdale Research and Education Center, University of Florida, IFAS, 3205 College Av.,
Fort Lauderdale, FL 33314, USA
7
Australian Tropical Herbarium, James Cook University, Cairns, Qld 4870, Australia
2
Received 9 September 2013; revised 14 November 2013; accepted for publication 14 November 2013
A unique obligate mutualism occurs between species of Fergusonina Malloch flies (Diptera: Fergusoninidae) and
nematodes of the genus Fergusobia Currie (Nematoda: Neotylenchidae). These mutualists together form different
types of galls on Myrtaceae, mainly in Australia. The galling association is species-specific, and each mutualism in
turn displays host specificity. This tritrophic system represents a compelling arena to test hypotheses about
coevolution between the host plants, parasitic nematodes and the fergusoninid flies, and the evolution of these
intimate mutualisms. We have a basic knowledge of the interactions between the host plant, fly and nematode in this
system, but a more sophisticated understanding will require a much more intensive and coordinated research effort.
Summaries of the known Fergusonina/Fergusobia species associations and gall type terminology are presented. This
paper identifies the key advantages of the system and questions to be addressed, and proposes a number of
predictions about the evolutionary dynamics of the system given our understanding of the biology of the mutualists.
Future research will profitably focus on (1) gall cecidogenesis and phenology, (2) the interaction between the fly larva
and the nematode in the gall, and between the adult female fly and the parasitic nematode, (3) the means by which
the fly and nematode life cycles are coordinated, (4) a targeted search of groups in the plant family Myrtaceae that
have not yet been identified as gall hosts, and (5) establishment and comparison of the phylogenetic relationships of
the host plants, fly species and nematodes. Recently derived phylogenies and divergence time estimation studies of
the Diptera and the Myrtaceae show that the fly family Fergusoninidae is less than half the age of the Myrtaceae,
discounting the hypothesis of cospeciation and coradiation of the fly/nematode mutualism and the plants at the
broadest levels. However, cospeciation may have occurred at shallower levels in the phylogeny, following the
establishment of the fly/nematode mutualism on the Myrtaceae. 2014 The Linnean Society of London, Biological
Journal of the Linnean Society, 2014, 111, 699718.
699
700
L. A. NELSON ET AL.
INTRODUCTION
Nematode
Parasitic
IN FLY
Fly
Eggs
Eggs
Juveniles
Oviposition
IN GALL
Juveniles
Eggs
Parthenogenetic
1st
Amphimictic +
Fertilised
preparasitic
2nd
Nematodes
into larvae
Larval
instars
3rd
Pupae
2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 699718
GALL
TYPES
701
FLY
Location
Locule type
Leaf
Petiole (A)
Unilocular
Multilocular
Unilocular
Multilocular
Unilocular
Multilocular
Multilocular
Unilocular
Flat (B)
Shoot bud
Flower
bud (G)
Axillary (C)
Terminal (D)
Stigma
Stamen (primordial
tissue)
Ovary
Gall form
2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 699718
702
L. A. NELSON ET AL.
Figure 2. Representative Fergusonina/Fergusobia gall forms. A, leaf pea galls (unilocular) from E. pauciflora; B, shoot
bud gall from M. dealbata; C, axial leaf bud gall from E. camaldulensis; D, flat leaf gall from E. leucoxylon; E, flower bud
gall from E. microcarpa; F, leafy leaf bud gall from E. aromaphloia; G, terminal leaf bud gall from E. obliqua. All galls
except A are multilocular. Note exit holes in C and G. Scale bars = 1 cm.
tritrophic plant/nematode/fly interaction, poses distinct challenges. To date, records have been collected
for about 200 tritrophic associations (Tables 2 and 3;
G. S. Taylor and K. A. Davies, unpubl. data).
Description of a Fergusobia nematode is usually
undertaken only when all taxonomically informative
stages of the life cycle have been obtained. Nematodes
are only found in locules when eggs or the fly larvae
are present. Obtaining the taxonomically important
life stages for the Fergusonina flies (larvae, pupae
and adult) is easier than for the Fergusobia nematodes. The fly larvae and pupae remain in the galls
for longer, and provided that third-stage larvae are
present, adult flies can usually be reared from the
galls. The cuticular dorsal shield is unique among
Diptera larvae. It varies between species, from comprising a few raised spicules (being almost absent) to
transverse rows of raised, sclerotized spicules to large
2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 699718
Flower bud
Eucalyptus spp.
E. pauciflora species-group
biseta Malloch
1932
brimblecombi
Tonnoir 1937
burrowsi Taylor
2004
carteri Tonnoir
1937
centeri Taylor
2004
curriei Tonnoir
1937
davidsoni
Tonnoir 1937
daviesae Nelson
& Yeates 2011
eucalypti
Malloch 1932
evansi Tonnoir
1927
flavicornis
Malloch 1925
frenchi Tonnoir
1937
giblindavisi
Taylor 2008
goolsbyi Taylor
2004
leaf galls
leaf galls
Flower bud
Unknown
Leaf bud
leaf galls
leafy leaf bud
Flower-bud
Flower-bud
Unknown
Unknown
atricornis
Malloch 1925
Gall type
Myrtaceous host
Fergusonina sp.
2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 699718
North coastal Qld
Mareeba (Qld)
Eastern Australia
Brisbane (Qld)
Cairns (Qld)
Emerald (Vic)
Canberra (ACT)
Adelaide (SA)
Adelaide (SA)
Canberra (ACT)
Cairns (Qld)
Cardwell (Qld)
Bodalla (NSW)
Sydney (NSW)
Canberra (ACT)
Distribution
Unknown
Unknown
Unknown
Unknown
Dorsal shield
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Fergusobia sp.
Table 2. Summary of described Fergusonina flies and Fergusobia nematodes, their myrtaceous host, gall type, distribution based on collection records and larval
dorsal shield type
703
leaf gall
Nodular, terminal or axial shoot bud
galls with fine pubescence
Unknown
E. pauciflora species-group
(Nelson & Yeates, 2011)
Unknown
E. pauciflora species-group
makinsoni
Taylor 2004
metrosiderosae
Taylor 2007
microcera
Malloch 1924
morgani Tonnoir
1937
newmani
Tonnoir 1937
nicholsoni
Tonnoir 1937
omlandi Nelson
& Yeates 2011
pescotti Tonnoir
1937
purcelli Taylor
2004
schefferae Taylor
2004
scutellata
Malloch 1925
syzygii Harris
1982
thomasi Taylor
2008
thornhilli
Nelson &
Yeates 2011
tillyardi Tonnoir
1937
Flower bud
Flower bud
Axillary bud
Unknown
Flower bud
Flower bud
Unknown
leaf gall
Terminal leaf
Axial shoot bud
lockharti
Tonnoir 1937
Flower bud
stem-tip
greavesi Currie
1937
Gall type
gurneyi Malloch
1932
Myrtaceous host
Fergusonina sp.
Table 2. Continued
Canberra
Naracoorte (SA)
Vic. (Currie, 1937)
India
Sydney (NSW)
Emerald (Vic)
Canberra (ACT)
Clare (SA)
Perth (WA)
Vic
New Zealand
Northern Qld
Mundaring (WA)
Canberra (ACT)
Distribution
Unknown
Unknown
Unknown
Unknown
Unknown
Small with
about 20 sparse raised sclerotized spicules
Unknown
Dorsal shield
curriei on E. camaldulensis)
(Fisher & Nickle, 1968)
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
gomphocephalae Davies
2012a
Unknown
Unknown
Unknown
Unknown
Fergusobia sp.
704
L. A. NELSON ET AL.
2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 699718
Unknown
Flower bud
2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 699718
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Unknown
Stigma gall
Unknown
Flower bud
Unknown
n/a
Unknown
Flower bud
Unknown
Unknown
Flower bud
Flat leaf
Unknown
Unknown
Unknown
williamsensis
Nelson &
Yeates 2011
Unknown
turneri Taylor
2004
Pimpama (QLD)
Sydney (NSW)
Mudgee (NSW)
Meningie (SA)
Mylor (SA)
Strathalbyn (SA)
Adelaide (SA)
Woodburn (NSW)
Adelaide (SA)
Goolwa (SA)
Canberra (ACT)
India
Philippines
Bulolo (PNG)
Adelaide (SA)
Coastal Qld
Grampians (Vic)
Coastal Qld
North coastal NSW
Absent
Absent
Absent
Bars of spicules
Unknown
Unknown
Unknown
pimpamensis
Davies 2013
minimus
Lisnawita 2013
floribundae
Davies 2013
diversifoliae
Davies 2013
delegatensae
Davies 2013
cosmophyllae
Davies 2013
microcarpae
Davies 2013
Unknown
705
706
L. A. NELSON ET AL.
Table 3. A list of Fergusonina eucalypt hosts sorted by the taxonomic treatment of Brooker, Slee & Connors (2006)
Species
Subgenus
Angophora costata
Angophora floribunda
Angophora subvelutina
Corymbia trachyphloia
Corymbia papuana
Corymbia tessellaris
Corymbia torelliana
Corymbia citriodora
Corymbia maculata
Corymbia abbreviata
Corymbia gummifera
Corymbia intermedia
Corymbia ptychocarpa
Eucalyptus acmenoides
Eucalyptus amygdalina
Eucalyptus coccifera
Eucalyptus elata
Eucalyptus nitida
Eucalyptus tenuiramis
Eucalyptus baxteri
Eucalyptus eugenioides
Eucalyptus ligustrina
Eucalyptus macrorhyncha
Eucalyptus delegatensis
Eucalyptus haemastoma
Eucalyptus pauciflora
Eucalyptus racemosa
Eucalyptus sieberi
Eucalyptus obliqua
Eucalyptus stricta
Eucalyptus planchoniana
Eucalyptus marginata
Eucalyptus diversifolia
Eucalyptus stellulata
Eucalyptus olsenii
Eucalyptus cloeziana
Eucalyptus coolabah
Eucalyptus pruinosa
Eucalyptus albens
Eucalyptus intertexta
Eucalyptus largiflorens
Eucalyptus microcarpa
Eucalyptus moluccana
Eucalyptus odorata
Eucalyptus polybractea
Eucalyptus populnea
Eucalyptus porosa
Eucalyptus crebra
Eucalyptus fibrosa
Eucalyptus melanophloia
Eucalyptus siderophloia
Eucalyptus baueriana
Eucalyptus fasciculosa
Eucalyptus polyanthemos
Eucalyptus leucoxylon
Eucalyptus melliodora
Eucalyptus sideroxylon
Eucalyptus yalatensis
Eucalyptus zopherophloia
Angophora
Angophora
Angophora
Corymbia
Corymbia
Corymbia
Corymbia
Corymbia
Corymbia
Corymbia
Corymbia
Corymbia
Corymbia
Eucalyptus
Eucalyptus
Eucalyptus
Eucalyptus
Eucalyptus
Eucalyptus
Eucalyptus
Eucalyptus
Eucalyptus
Eucalyptus
Eucalyptus
Eucalyptus
Eucalyptus
Eucalyptus
Eucalyptus
Eucalyptus
Eucalyptus
Eucalyptus
Eucalyptus
Eucalyptus
Eucalyptus
Eucalyptus
Idiogenes
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Section
Subsection
Apteria
Blakearia (ghost gums)
Blakearia (ghost gums)
Cadagaria
Politaria (spotted gums)
Politaria (spotted gums)
Rufaria (red bloodwoods)
Rufaria (red bloodwoods)
Rufaria (red bloodwoods)
Rufaria (red bloodwoods)
Amentum (white mahoganies)
Aromatica (peppermints)
Aromatica (peppermints)
Aromatica (peppermints)
Aromatica (peppermints)
Aromatica (peppermints)
Capillulus (stringy barks)
Capillulus (stringy barks)
Capillulus (stringy barks)
Capillulus (stringy barks)
Cineraceae
Cineraceae
Cineraceae
Cineraceae
Cineraceae
Eucalyptus (the ashes)
Eucalyptus (the ashes)
Insolitae
Longistylus
Longistylus
Longitudinales
Nebulosa
Adnataria
Adnataria
Adnataria
Adnataria
Adnataria
Adnataria
Adnataria
Adnataria
Adnataria
Adnataria
Adnataria
Adnataria
Adnataria
Adnataria
Adnataria
Adnataria
Adnataria
Adnataria
Adnataria
Adnataria
Adnataria
Bisectae
Bisectae
(the
(the
(the
(the
(the
(the
(the
(the
(the
(the
(the
(the
(the
(the
(the
(the
(the
(the
(the
(the
(the
boxes
boxes
boxes
boxes
boxes
boxes
boxes
boxes
boxes
boxes
boxes
boxes
boxes
boxes
boxes
boxes
boxes
boxes
boxes
boxes
boxes
and
and
and
and
and
and
and
and
and
and
and
and
and
and
and
and
and
and
and
and
and
ironbarks)
ironbarks)
ironbarks)
ironbarks)
ironbarks)
ironbarks)
ironbarks)
ironbarks)
ironbarks)
ironbarks)
ironbarks)
ironbarks)
ironbarks)
ironbarks)
ironbarks)
ironbarks)
ironbarks)
ironbarks)
ironbarks)
ironbarks)
ironbarks)
Series
Arboreae
Frutices
Apicales
Apicales
Apicales
Apicales
Apicales
Apicales
Apicales
Apicales
Apicales
Apicales
Apicales
Apicales
Apicales
Apicales
Apicales
Terminales
Terminales
Terminales
Terminales
Terminales
Terminales
Destitutae (pith glands absent)
Glandulosae (pith glands present)
Aquilonares
Aquilonares
Buxeales
Buxeales
Buxeales
Buxeales
Buxeales
Buxeales
Buxeales
Buxeales
Buxeales
Siderophloiae
Siderophloiae
Siderophloiae
Siderophloiae
Heterophloiae
Heterophloiae
Heterophloiae
Melliodorae
Melliodorae
Melliodorae
Subulatae
Accedentes
2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 699718
707
Table 3. Continued
Species
Subgenus
Section
Subsection
Series
Eucalyptus platypus
Eucalyptus loxophleba
Eucalyptus
gomphocephala
Eucalyptus lesouefii
Eucalyptus blakelyi
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Bisectae
Bisectae
Bolites
Erectae
Loxophlebae
Symphyomyrtus
Symphyomyrtus
Eucalyptus dealbata
Symphyomyrtus
Eucalyptus tereticornis
Symphyomyrtus
Eucalyptus lockyeri
Symphyomyrtus
Eucalyptus camaldulensis
Symphyomyrtus
Eucalyptus rudis
Symphyomyrtus
Eucalyptus cupularis
Symphyomyrtus
Dumaria
Exsertaria
gums)
Exsertaria
gums)
Exsertaria
gums)
Exsertaria
gums)
Exsertaria
gums)
Exsertaria
gums)
Exsertaria
gums)
Eucalyptus cosmophylla
Eucalyptus robusta
Symphyomyrtus
Symphyomyrtus
Incognitae
Latoangulatae
Eucalyptus interstans
Symphyomyrtus
Eucalyptus
parramattensis
Eucalyptus bridgesiana
Eucalyptus globulus
Eucalyptus johnstonii
Eucalyptus dalrympleana
Eucalyptus viminalis
Eucalyptus aromaphloia
Eucalyptus nicholii
Eucalyptus aggregata
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Liberivalvae (red
from the ovary
Liberivalvae (red
from the ovary
Maidenaria
Maidenaria
Maidenaria
Maidenaria
Maidenaria
Maidenaria
Maidenaria
Maidenaria
Eucalyptus ovata
Symphyomyrtus
Maidenaria
Triangulares
Eucalyptus
Eucalyptus
Eucalyptus
Eucalyptus
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Symphyomyrtus
Maidenaria
Platysperma
Platysperma
Sejunctae
Triangulares
mannifera
brevifolia
confluens
cladocalyx
Rufispermae
Erythroxylon
Erythroxylon
Erythroxylon
Phaeoxylon
Rostratae
Singulares
Subexsertae
(white
gums)
Annulares
(red
mahoganies)
PLANT
HOST DIVERSITY
Euryotae
Euryotae
Euryotae
Euryotae
Euryotae
Triangulares
Triangulares
Triangulares
Bridgesianae
Globulares
Semiunicolores
Viminales
Viminales
Acaciiformes
Acaciiformes
Foveolatae
(swamp
gums)
Foveolatae
(swamp
gums)
Microcarpae
2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 699718
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L. A. NELSON ET AL.
Figure 3. Chronogram of the tribes of Myrtaceae adjusted from Thornhill et al. (2012). Shaded tribes highlight
Fergusonina hosts and show that no sister tribes in Myrtaceae have been found to host the flies. The figures next to each
tribe name indicate how many species have been recorded as hosts versus the number of species recognized in the tribe.
*Tribes that do not have any representative taxa in Australia.
2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 699718
GALL
PHENOLOGY
709
CECIDOGENESIS
The process of gall formation, or cecidogenesis, is a
neoplastic outgrowth of plant tissue as a defensive
mechanism following herbivory (Schick & Dahlsten,
2003). It involves complex interactions between
plants and causative organisms, with highly specific
reciprocal adaptations between plant host and gallinducer (e.g. Stone & Schnrogge, 2003; Raman,
2011). The chemical interactions between gallforming insects and their host plants are poorly
understood (Raman, 2010). Gall-forming insects
commonly show preference for undifferentiated
meristematic plant tissue as oviposition sites (e.g.
Mani, 1964; Fritz et al., 1987; Price, Fernandes &
Waring, 1987; Raman, 2010). Little is known about
how Fergusonina flies select an oviposition site.
Their oviposition behaviour may be influenced by a
combination of visual and olfactory cues including
semiochemicals and plant hormones (auxins, e.g.
indole-acetic acid), which are particularly prevalent
in meristematic tissue (Raman, 2010). Oviposition
preference in the shoot fly (Atherigona soccata) in
seedling sorghum is positively correlated with nitrogen content of the growing tip (Ogwaro & Kokwaro,
1981). Most Fergusonina/Fergusobia galls occur
on young foliage, presumably with higher nitrogen
content (Larsson & Ohmart, 1988; Edwards &
Wanjura, 1991).
Experimental injection of juvenile Fergusobia
nematodes into shoot buds (Giblin-Davis et al., 2001b)
led to some gall and nematode development. Thus,
the nematode appears to induce gall development, but
the fly larva is responsible for the internal structure
of the gall. Nematodes failed to develop in vitro on
callus culture (Head, 2008). Given their strong stylet,
it is most likely that Fergusobia nematodes feed on
plant material (Giblin-Davis et al., 2001b, 2004a),
although Currie (1937) suggested that they may also
feed on excretions of the co-occurring fly larvae.
In recent years, considerable efforts have been
made to understand the process of cecidogenesis
in gall-forming pest nematodes. All plant-parasitic
nematode genomes examined to date (e.g. Bert et al.,
2008; Bird, Williamson & Abad, 2009; Dieterich &
Sommer, 2009; van Megen et al., 2009; Kikuchi et al.,
2011) have genes coding for secreted enzymes that
degrade cell walls, which may have originated from
horizontally transferred bacterial or fungal genes
2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 699718
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L. A. NELSON ET AL.
COORDINATION
Clearly, the life cycles of the fly and the nematode are
closely coordinated (Fig. 1). The cues which regulate
this coordination and its evolution are unknown, but
may be hormonal. For example, in the beetle parasite
Contortylenchus brevicomi, fourth-stage juvenile
nematodes were stimulated to moult while within the
body cavity of the host larva (Gibb & Fisher, 1986,
1989), but ecdysis was inhibited by high concentrations of juvenile hormone in the host, and nematodes
moulted once they left the larva. Fergusobia nematodes parasitic in the pupae of the flies may be
stimulated to moult by the high concentrations of
ecdysteroid known to be present in dipteran puparia
(Walker & Denlinger, 1980), which could be tested in
vitro.
Between one and 50 juvenile nematodes were associated with Fergusonina eggs deposited in flower buds
(Giblin-Davis et al., 2004a). Apparently, nematodes
are deposited passively with eggs during oviposition
(Currie, 1937) and it is not clear whether the fly is
able to regulate the number of nematodes deposited
with each egg.
Nematodes occur only in female larvae, pupae and
flies (Davies et al., 2001; Giblin-Davis et al., 2001b;
Scheffer et al., 2013). Sex pheromones may be recognized in the selection of female Fergusonina larvae
and pupae. Nematodes select for female hosts in other
systems, including the tylenchid Sphaerularia bombi
which only invades queen bumblebees (Poinar &
Van Der Laan, 1972) and the fig-waspnematode
tritrophic interactions in Ficus sycones (Krishnan
et al., 2010).
2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 699718
711
FLYNEMATODE
COSPECIATION
Cospeciation (co-cladogenesis) between closely interacting organisms has been studied extensively over
the past several decades, resulting in the common
view that cospeciation is most likely in cases of vertical (rather than horizontal) transmission of the
interaction (Moran & Baumann, 2000; Page, 2003;
Hosokawa et al., 2006). The Fergusonina/Fergusobia
mutualism appears to be an exceptional candidate for
cospeciation given the apparent strict vertical transmission of nematodes between fly generations (Davies
et al., 2010b). However, recent molecular evidence
suggests that large multilocular galls can have multiple conspecific fly foundresses, potentially allowing
for horizontal transfer of nematodes between offspring of different females (Purcell, 2012). Switching
2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 699718
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L. A. NELSON ET AL.
SPECIATION
Host range may affect diversification rates of ecologically specialized gall-forming insects (Hardy & Cook,
2010). In the case of the Fergusonina/Fergusobia
mutualisms, most are highly specialized and found
only on one or a few closely related host plant species
(Davies et al., 2010b; Nelson et al., 2011a), suggesting
that speciation events typically occur in conjunction
with a shift to a new host plant species or tissue type.
Because the female Fergusonina fly chooses new
oviposition sites for galling, it is the behaviour and
host plant/tissue specificity of the flies that provide
the initial micro-evolutionary variation upon which
speciation processes can act. The ability of the nematodes both to initiate and to function within the gall
is critical and a major source of selection on the
oviposition choices made by the female flies. A female
fly that oviposits onto a new plant species or plant
tissue type in which the nematodes cannot function
normally will have lower fitness than the flies choosing their normal host.
Little work has been undertaken on host choice for
the fly/nematode mutualism. In the only work published to date, Wright et al. (2013) made a series
of no-choice oviposition and development tests to
assess host use by the F. turneri/F. quinquenerviae
mutualism in Florida. Oviposition and gall develop-
2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 699718
713
Figure 4. Dendrogram of the eucalypts based on A. H. Thornhill et al. (unpubl. data) showing how the major subgenera
and sections are related to each other and where the concentration of Fergusonina host species occurs in the phylogeny.
CONCLUSIONS
While understanding of the Fergusonina/Fergusobia
association is limited, its life cycle is established, and
it is known that flies and nematodes have a complex
and obligatory mutualism, each of which is generally
host-specific. At present, little is known of fly behaviour, host choice, the process of cecidogenesis, factors
determining host resistance or the selection pressures
operating on the mutualism. However, the genetic
tools needed to analyse many of these are now available, and models against which hypotheses can be
tested are becoming increasingly available.
Plant-feeding insects comprise an extraordinary
proportion of extant biodiversity (Strong, Lawton &
Southwood, 1984; Mitter, Farrell & Wiegmann, 1988;
Schoonhoven, van Loon & Marcel, 2005), and provide
important and compelling examples of evolution.
Given the complex and obligate nature of the
Fergusonina/Fergusobia mutualism, and their relationships with their myrtaceous hosts, the development of robust, dated, phylogenies for all three
trophic levels will provide a unique study system for
cospeciation and coevolution. A robust phylogeny
of both flies and nematodes at deep levels is necessary
for co-phylogenetic comparisons, but is only available for the flies. Such phylogenies will also allow
2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 699718
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L. A. NELSON ET AL.
ACKNOWLEDGEMENTS
Special thanks to Ted and Barb Center, Paul Pratt,
Greg Wheeler, Scott Blackwood, Phil Tipping, Susan
Wright, Weimin Ye and Dorota Porazinska among
many others at the USDA IPRL (Invasive Plant
Research Lab) and the University of Florida, IFAS
FLREC in Fort Lauderdale, Florida, for their help and
support during studies of this amazing group of flies
and nematodes for deployment as a biological control
agent against M. quinquenervia in the United States.
Some of the research summarized in this article was
supported by USDA Special Grants in Tropical and
Subtropical Agriculture (CRSR-99-34135-8478 and
CRSR-03-34135-14078) to R.G.D.; and by Australian
Biological Resources Studies grants to K.A.D.
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