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Tachinidae: Evolution, Behavior, and Ecology

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Tachinidae are one of the most diverse and ecologically important families in the order Diptera. As parasitoids, they are important natural enemies in most terrestrial ecological communities, particularly as natural enemies of larval Lepidoptera. Despite their diversity and ecological impact, relatively little is known about the evolution and ecology of tachinids, and what is known tends to be widely dispersed in specialized reports, journals, or texts. In this review we synthesize information on the evolutionary history, behavior, and ecology of tachinids and discuss promising directions for future research involving tachinids. We provide an overview of the phylogenetic history and geographic diversity of tachinids, examine the evolution of oviposition strategies and host associations, review known mechanisms of host location, and discuss recent studies dealing with the ecological interactions between tachinids and their hosts. In doing so, we highlight ways in which investigation of these parasitoids provides insight into such topics as biogeographic patterns of diversity, the evolution of ecological specialization, the tritrophic context of enemy-herbivore interactions, and the role of host location behavior in shaping host range.
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10.1146/annurev.ento.51.110104.151133
Annu. Rev. Entomol. 2006. 51:525–55
doi: 10.1146/annurev.ento.51.110104.151133
Copyright
c
2006 by Annual Reviews. All rights reserved
First published online as a Review in Advance on August 31, 2005
TACHINIDAE
: Evolution, Behavior, and Ecology
John O. Stireman, III,
1
James E. O’Hara,
2
and D. Monty Wood
2
1
Department of Biological Sciences, Wright State University, Dayton, Ohio 45435;
email: john.stireman@wright.edu
2
Invertebrate Biodiversity, Agriculture and Agri-Food Canada, Ottawa, Ontario,
K1A 0C6 Canada; email: oharaj@agr.gc.ca, wooddm@agr.gc.ca
KeyWords
Diptera, parasitoid, biodiversity, host range, host location
Abstract Tachinidae are one of the most diverse and ecologically important fami-
lies in the order Diptera. As parasitoids, they are important natural enemies in most ter-
restrial ecological communities, particularly as natural enemies of larval Lepidoptera.
Despite their diversity and ecological impact, relatively little is known about the evo-
lution and ecology of tachinids, and what is known tends to be widely dispersed in
specialized reports, journals, or texts. In this review we synthesize information on
the evolutionary history, behavior, and ecology of tachinids and discuss promising
directions for future research involving tachinids. We provide an overview of the phy-
logenetic history and geographic diversity of tachinids, examine the evolution of ovipo-
sition strategies and host associations, review known mechanisms of host location, and
discuss recent studies dealing with the ecological interactions between tachinids and
their hosts. In doing so, we highlight ways in which investigation of these parasitoids
provides insight into such topics as biogeographic patterns of diversity, the evolution of
ecological specialization, the tritrophic context of enemy-herbivore interactions, and
the role of host location behavior in shaping host range.
INTRODUCTION
The Tachinidae are one of the most speciose families of Diptera, with approxi-
mately 10,000 described species worldwide (71). One of the few traits that unites
this diverse assemblage of flies is that all tachinids (with known life histories) are
parasitoids of insects and other arthropods. In this respect, they are second only
to the parasitic Hymenoptera (e.g., Ichneumonoidea, Chalcidoidea) in diversity
and ecological importance as insect parasitoids. Because of their predominance
as parasitoids of the larval stage of Lepidoptera and other major groups of insect
herbivores (e.g., Heteroptera, Scarabaeidae, Symphyta, Chrysomelidae), tachinids
often play significant roles in regulating herbivore populations and structuring eco-
logical communities, both natural and managed. On the order of 100 species have
been employed in biological control programs of crop and forest pests, and many of
these programs have been met with partial or complete success (49, 50). However,
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526 STIREMAN
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introduced tachinids have also been implicated in devastating effects on nontarget
organisms (17).
Tachinids are found in nearly all terrestrial environments throughout the world
including deserts, forests, grasslands, mountains, and tundra, and at times may
constitute a large proportion of flies observed in particular habitats. In addition, they
are widely regarded as a relatively recent, actively radiating group of insects that we
may be seeing in the full climax of evolutionary diversification (28). Despite this
abundance, diversity, and ecological importance, relatively little is known about
the evolutionary history, ecology, and behavior of tachinids. Even basic biological
information on hosts, mating systems, and habitat requirements is known for fewer
than half of the species in the most well-studied regions (i.e., Europe) (90). Most of
our knowledge of tachinids comes from an extensive history of studies concerned
with their potential application in controlling pests in managed agricultural and
forest systems (50). However, owing to their ecological importance in natural
systems as parasitoids of herbivorous insects, tachinids are attracting increasing
attention from basic ecologists (47, 143). Novel host location mechanisms of
certain species and associated implications for host-parasitoid coevolution have
also attracted recent attention (e.g., phonotaxis to sexual calls of Orthoptera by the
tribe Ormiini) (48). In addition, recent systematic analyses of morphology and at
least one molecular phylogenetic study have begun to provide an initial foundation
for understanding their evolutionary relationships, historical biogeography, and
the evolutionary development of their host associations. In this review, we provide
an overview of tachinid evolution and ecology, focusing on recent literature. We
further examine four main areas in which we believe research on tachinids may be
particularly rewarding: (a)evolution and biogeography of Tachinidae, (b)evolution
of oviposition strategies and host associations, (c) behavioral mechanisms of host
location, and (d) ecological interactions between tachinids and their hosts. These
represent but a few of the many potential topics that could be discussed with
regard to the Tachinidae. However, we hope that a review of these aspects of
tachinid biology illustrates the remarkable diversity within the family and offers
insight into more general issues in evolutionary biology, ecology, and behavior.
OVERVIEW OF TACHINID BIOLOGY
Tachinids are muscoid calyptrate Diptera belonging to the superfamily Oestroidea
along with groups such as the flesh flies (Sarcophagidae), bottle flies (Calliphori-
dae), and bot flies (Oestridae). Tachinids exhibit an impressive diversity of mor-
phologies (Figures 1 and 2), ranging in size over an order of magnitude from the
diminutive (2 mm; e.g., Siphona spp.) to the impressively large (more than 20
mm; e.g., Trixodes obesa). A number of species are brightly colored with yellow,
black, orange, and/or red markings, possibly mimicking aculeate Hymenoptera.
Others are decorated with vivid metallic green, blue, or other tints (e.g., the
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visually impressive Australian Rutiliini). However, many species, especially those
belonging to the diverse subfamily Exoristinae, tend to be rather small, gray or
blackish, and superficially nondescript. Closer inspection of these forms reveals
adiverse array of morphologies and patterning, representing some of the most
impressive radiations of tachinids, such as in the tribes Blondeliini, Eryciini, and
Voriini.
All tachinid species are parasitoids, more specifically internal (endo-) para-
sitoids of other arthropods. As is typical for parasitoids, tachinids usually kill their
hosts (but there are exceptions) (40). Although many tachinids emerge from the
pupal stage of their hosts, none is known to attack pupae nor do any species attack
the egg stage of their hosts. Most species of tachinids attack larval hosts, but a sig-
nificant fraction, perhaps 5% to 10% of species, attack adults. Larval development
is usually completed in one to three weeks, except for species that diapause in the
host, where it can be prolonged over many months. Depending on the tachinid
species, larvae develop either singly or gregariously and either pupate in the dead
host or leave the host remains to pupate in soil litter.
Unlike parasitic Hymenoptera, tachinids lack a primitive piercing oviposi-
tor. Thus, with the exception of a few groups in which piercing structures have
evolved from modified sternites (e.g., most Phasiinae, many Blondeliini), ta-
chinids must deposit eggs externally on or near the host, and the newly hatched
larva must gain entry into the host. This lack of an ovipositor also prevents
the injection of paralytic poisons, mutualistic polyDNA viruses, and other ac-
cessory substances that immobilize the host and/or its immune system. As a
result, tachinids are classified as koinobiont parasitoids (9), that is, they allow
their host to continue to feed and grow while they develop inside it rather than
arresting its development in some way (as do idiobionts). Tachinids attack a
wide range of hosts, comparable to that of the more diverse parasitic wasps
(36) (Figure 3). The most commonly used hosts are phytophagous insects, pri-
marily Lepidoptera, Coleoptera (Scarabaeidae and Chrysomelidae), Hymenoptera
(Symphyta), Heteroptera, and Orthoptera. However, hosts in at least six additional
insect orders, including Blattodea, Dermaptera, Diptera, Embioptera, Mantodea,
and Phasmida, are attacked. Several genera of tachinids attack noninsect arthro-
pods, specifically centipedes (e.g., tachinid genera Loewia and Eloceria) and scor-
pions (161). There is a single record of the parasitism of a spider (157). This great
breadth of host use by the family is accompanied by broad host ranges in some
tachinid species. Unlike parasitic Hymenoptera with similar life histories (koino-
biont endoparasitoids) that tend to be highly host specific, many tachinid species are
polyphagous, and a number have been reared from dozens of hosts in multiple fam-
ilies (37). At the extreme end, the tachinid Compsilura concinnata attacks almost
200 species of hosts in dozens of families and even multiple orders (Lepidoptera,
Hymenoptera, and Coleoptera) (8). The striking variation in host range among
species of Tachinidae makes the group particularly well suited for investigating
the evolution, ecological consequences, and behavioral basis of host specificity.
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Although this review focuses on the evolutionary history of tachinids and their
ecological interactions with hosts, we draw attention to some aspects of the adult
biology of tachinids that have received little attention. Adult tachinids can be
found in most habitats, on leaves, tree trunks, flowers, rocks, or the ground. They
are typically, but not always, diurnal or crepuscular and extremely active. Little
is known about the mating behavior of tachinids aside from the general sexual
aggregation sites of many species (e.g., hilltops, tree trunks) (1, 164). Adults of
certain groups such as Phasiinae and Tachinini are often observed at flowers and
may function as pollinators for a wide diversity of plant taxa, but their importance
in this respect has been largely unexplored. At least one highly specific tachinid
pollinates orchids in the genus Trichoceros via pseudocopulation, in which the
female tachinid mimicking flowers lure tachinid males to attempt copulation and
incidentally acquire pollinia (33). The importance of adult resources such as nectar,
salts, leaf exudates, or potential sources of protein (e.g., pollen) is poorly known,
as are patterns of adult dispersal.
EVOLUTION AND DIVERSIFICATION OF TACHINIDAE
Phylogenetic Relationships
The early history of the Tachinidae is poorly understood. There are surprisingly
few fossils, the sister group has not been determined, the region of early evolution
is uncertain, and basal relationships within the family are still under debate. De-
spite such fertile ground for discoveries of significance, this huge taxon has been
understudied in favor of smaller families that are more amenable to phylogenetic
investigation on a global scale.
The Tachinidae are the largest family of the Oestroidea, which includes, in addi-
tion to the Tachinidae, the Calliphoridae, Mystacinobiidae, Oestridae, Rhinophori-
dae, and Sarcophagidae. The relationships between these families have been ex-
plored by several authors, but a strongly supported phylogenetic tree remains
elusive (89, 108, 118). The sister group to the Tachinidae has been postulated as
the Rhinophoridae (89, 163) or Sarcophagidae (108, 118). Earlier regional cata-
logs of Tachinidae included the rhinophorids as a tachinid subfamily (54, 125), but
this small group of flies has been universally regarded as a distinct family since
Crosskey’s (29) review of the group.
The fossil history of the entire oestroid lineage is markedly sparse and gener-
ally uninformative about the origin of the Oestroidea or Tachinidae. The oldest
potential fossil in this lineage is a collection of puparia from Alberta, Canada,
dating from the Upper Cretaceous. This specimen was originally assigned to
the Calliphoridae (88) but is now unplaced beyond the Schizophora (52). All
other known fossils of Oestroidea are Eocene or younger, and the oldest ta-
chinid is described from an Eocene compression fossil from the United States
(41).
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The monophyly of the Tachinidae is well established on the basis of at least
two synapomorphies, a well-developed subscutellum in the adult and the labrum
extended forward and broadly fused to the rest of the cephalopharyngeal skeleton
in the first instar (108, 117, 154, 164). Obligate endoparasitism of arthropods is a
universal characteristic of the Tachinidae, but it has been suggested that this may
not be a suitable character for inferring monophyly (108).
Early attempts to classify the Tachinidae into genera, tribes, and subfamilies
were based mostly on the external features of adults. This was the principal modus
operandi of the prolific C.H.T. Townsend, who proposed 1555 new species names
and 1491 new generic names of Tachinidae throughout a career spanning the
1880s to 1940s (7). Unfortunately, there is much homoplasy in the external char-
acters of tachinids, and most early authors, including Townsend, placed too much
emphasis on such characters in the formation of their suprageneric classifica-
tions (111). Homoplasy within the family prompted Crosskey (28, p. 8) to write,
“The Tachinidae...are certainly a group in which acquisition or loss of partic-
ular characters in different evolutionary lines has given rise to much confusing
resemblance....Few groups of Diptera give more difficulty in classification at the
suprageneric level....”
Townsend’s (151) classification of the Tachinidae also suffered from his propen-
sity for describing monotypic genera (one species per genus). Indeed, the Neotrop-
ical Tachinidae are still largely arranged according to Townsend’s classification
(54). The Neotropical region has such an overwhelming number of small and al-
most meaningless genera that its fauna is currently almost impossible to compare
with the more integrated classifications of other regions (22, 28, 30, 69, 105).
Most authors now recognize four tachinid subfamilies, the Exoristinae,
Dexiinae, Phasiinae, and Tachininae (68, 69, 105, 154, 164). This is partly because
of advancements in our understanding of tachinid relationships and partly because
of a common desire to use a classification of convenience until a better classifica-
tion is proposed. The characters that led Townsend and others astray still pose huge
problems for modern systematists. However, the four subfamilies of Tachinidae
are not entirely arbitrary in their composition. The Dexiinae are widely accepted
as monophyletic because of derived features in the male genitalia (112, 153, 164).
The Phasiinae comprise a morphologically diverse assemblage of species that was
historically united chiefly because of their parasitism of Heteroptera (26). How-
ever, more recently the monophyly of the Phasiinae has been based primarily on
a feature of the male genitalia (112, 153). There are some features that unite most
Exoristinae and other features that unite most Tachininae such that these groups
have some practical value, but neither is demonstrably monophyletic on morpho-
logical grounds. Nevertheless, Tschorsnig (153) concluded that the Exoristinae are
probably monophyletic and Stireman (140) provided some molecular evidence that
this subfamily may be largely monophyletic.
A complicating factor in resolving the relationships between tachinid subfami-
lies, in addition to the possible para- or polyphyly of the Exoristinae and Tachini-
nae, is competing interpretations of oviparity/ovolarviparity and egg morphology
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in the different subfamilies. The oviparous condition (the laying of unincubated
eggs that have no appreciable embryonic development) is presumed to be primitive
in the Tachinidae and is found in all Exoristini and Winthemiini, a few Blondeliini
and Eryciini (all in Exoristinae), all Phasiinae (excluding Eutherini and Strongy-
gastrini) (105, 164), and perhaps a few other as yet unexamined groups. The
ovolarviparous condition (the laying of incubated eggs containing well-developed
larvae) is present in the rest of the Exoristinae and all members of Dexiinae and
Tachininae. Depending upon whether ovolarviparity is thought to have arisen once
or multiple times changes the possible relationships among the subfamilies. Wood
(162) argued that ovolarviparity is associated with complex modifications of the
female reproductive system and probably evolved once. Other authors have taken
the view that ovolarviparity developed at least twice, based in large measure
on egg morphology, leading to other phylogenetic interpretations: Herting (66,
67) postulated the intersubfamilial relationships as Phasiinae + Exoristinae and
Tachininae + Dexiinae, Richter (112) modified this interpretation into Phasiinae +
(Exoristinae + (Tachininae + Dexiinae)), and Shima (129) proposed Phasiinae +
Dexiinae and Exoristinae + Tachininae. Under the scheme of Herting (66, 67),
the Tachinidae diverged early into two lineages, one in which the upper surface of
the egg is thickened and convex and the lower surface is membranous (termed a
planoconvex egg in tachinid literature) (Phasiinae + Exoristinae) and the other in
which the whole egg is essentially membranous (Tachininae + Dexiinae).
Tachinid tribes are still undergoing refinement and reorganization as their phylo-
genetic affinities become better understood. Systematic studies have been focused
generally on genera and species, so there have been few revisions of regional or
world faunas at the tribal level in recent decades. Significant tribal revisions dur-
ing the past 30 years have dealt with the Rutiliini (27), Uramyini (56), Blondeliini
(162), Siphonini (5, 6, 101), Dexiini (11), Winthemiini (130), and Polideini (102).
Interestingly, the two large tribes Goniini (Exoristinae) and Siphonini (Tachininae)
are each recognized as monophyletic only on the basis of internal structures: the
Goniini producing microtype eggs and the Siphonini having two rather than the
usual three spermathecae in females. The monophyly of many tribes has yet to be
investigated and the classification of Neotropical Tachinidae at all taxonomic lev-
els is in great need of modernization. Further advances in the global suprageneric
classification of the Tachinidae will benefit from integrating information from the
study of eggs (45), first instars (100, 113–115, 149, 151), puparia (166), female
terminalia (63), male terminalia (153, 156), molecular sequences (140), and host
associations (8, 55, 131), coupled with a cautious interpretation of the external
morphology of adults.
Diversity and Zoogeography
The Tachinidae are found worldwide and are one of the largest, if not the largest,
families of Diptera. The distribution of Tachinidae by region is shown in Table 1,
based on a recent enumeration of the genera (103) and variously dated sources of
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TABLE 1 Distribution of tachinid genera and species by biogeographic region
Number World Neotropical
a
Nearctic
a
Palearctic Afrotropical Oriental Australasian
b
Species 9899
c
2864
d
1345
e
>1600
f
1006
g
725
h
808
i
Genera
j
1530 822 303 404 213 266 228
Endemic genera 1130
k
644 61 153 93 54 125
% Endemic genera 78% 20% 38% 44% 20% 55%
Genera shared between regions
l
Neotropical 25
m
173 (102) 70 (1) 40 (0) 48 (0) 40 (0)
Nearctic 133 (38) 50 (1) 72 (1) 43 (0)
Palearctic 98 (14) 171 (55) 71 (1)
Afrotropical 96 (12) 61 (1)
Oriental 92 (20)
a
For the purposes of this paper, the boundary between the Nearctic and Neotropical regions is taken as the United States/Mexico border to correspond with the geographic
coverage of the catalogues by Guimarves (54) and O’Hara & Wood (105). The true boundary between these regions is in southern Mexico (51).
b
Australasian and Oceanian regions.
c
Data from Reference 71.
d
Data from Reference 54.
e
Data from Reference 105.
f
Data from Reference 154.
g
Data from Reference 71.
h
Data from Reference 28.
i
Data from Reference 22.
j
Data from Reference 103.
k
Total number of genera found in only one region.
l
Left number is total number of genera shared with another region; right number in parentheses is number of genera unique to two regions (data from Reference 103).
m
Number of genera found in all regions.
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species diversity (22, 28, 30 54, 105, 154). The species numbers are especially
deceptive because only the faunas of the Palearctic and Nearctic regions are rea-
sonably well known, with perhaps 90% of their actual faunas documented. The
huge number of species recorded from the Neotropical region, which accounts for
nearly one third of the described species of Tachinidae (Table 1), is but a portion
of the total, as evidenced from the many specimens of new species that abound
in collections. Similarly, the seemingly small faunas of the Afrotropical, Oriental,
and Australasian regions are understudied and likely highly diverse. The continent
of Australia (the largest land mass in the Australasian region), with a relatively
small described fauna of nearly 500 species (22), was recently estimated to have a
tachinid fauna “roughly in the order of 3500–4000 species” (104, p. 10). Consid-
ering the understudied nature of the world’s tachinid fauna, it is possible that only
half of the species have been described.
The geographic distribution of the Tachinidae is in agreement with the meager
fossil history of the family in failing to show evidence of a pre-Tertiary existence.
The most obvious indication of an earlier origin would be sister group relation-
ships among Southern Hemisphere tachinids, thereby suggesting a vicariance of
ancient faunas in the late Cretaceous or early Cenozoic. Most likely such relation-
ships would be seen at the generic level, but there are no genera unique to South
America, Africa, and Australia or to South America and Australia (Table 1). Only
one genus, Anacamptomyia Bischof, is known exclusively from the Afrotropi-
cal and Australasian regions (Table 1), but this apparent disjunction has not been
studied and the tachinid fauna of the intervening Oriental region is inadequately
known. Cort´es (25) postulated a relationship between the South American tribe
Trichoprosopini and the New Zealand tribe Occisorini, but that association has not
been explored in a phylogenetically rigorous manner.
There is no evidence from which to infer the region of origin of the Tachinidae.
From a zoogeographic perspective, the Tachinidae have radiated with surprising
thoroughness throughout the world. The faunas of adjacent regions show signif-
icant overlap in generic composition (Table 1) and all regions are diverse in the
major lineages. However, each region also supports a significant endemic fauna.
Most notable in this respect are the diverse tribes Rutillini and Occisorini, the first
an essentially Australasian group (22) and the second endemic to New Zealand
(34), both of which presumably diversified in situ after early colonization events.
New Zealand has remained far removed from Australia throughout the Cenozoic,
and as a result its tachinid fauna is highly endemic and apparently descended from
few ancestors (34). The fauna of Madagascar, on the other hand, although rich in
Tachinidae, has proportionally a far less endemic fauna than New Zealand (71).
The Neotropical region boasts an endemic fauna of 644 genera, fully 78% of its
genera (Table 1), but this is in part an artifact of the oversplit generic classification.
Nevertheless, the Neotropical fauna is huge and diverse and tachinids must have
had a long history there. The water gap between North and South America that
closed in the Pliocene and resulted in the “great American biotic interchange,” so
evident in the New World megafauna (136), seems to have functioned more as a
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“filter bridge” than as a barrier for tachinids during the Tertiary (101). A similar
pattern of progressive enrichment probably took place in Australia as that continent
and associated islands slowly edged toward the island archipelagos of Southeast
Asia in the late Cenozoic. In the Northern Hemisphere, intermittent land connec-
tions between North America and Eurasia across the North Atlantic and through
Beringia at various times during the Cenzoic (87) must surely have provided key
pathways between the Old and New Worlds for Tachinidae, if indeed the family is
too recent to have used Gondwanan corridors between southern continents.
Latitudinal Considerations
Certain parasitoid taxa such as the Ichneumonidae apparently lack a gradient of
increasing diversity toward the tropics found in most insect groups (73). Hypothe-
ses to explain these unusual patterns of diversity have suggested that specialized
parasitoid populations experience difficulty persisting in the tropics because of re-
source fragmentation (73), a preponderance of chemically defended “nasty” hosts
(46), and other factors. Although the tropical faunas of Tachinidae are not well
known in the Old World, the Neotropical Region clearly harbors a fauna much
larger than those in the temperate latitudes of the Nearctic and Palearctic regions.
As an example of this diversity, Janzen & Hallwachs’ (74) Lepidoptera-rearing pro-
gram in Costa Rica indicates that approximately 330 species of tachinids (>80%
undescribed) have been reared from caterpillars at a single tropical forest site.
The reasons behind these disparate diversity patterns for Ichneumonidae and Ta-
chinidae are not well explored, but the generally greater polyphagy and perhaps
reduced susceptibility of tachinids to host chemical defenses may be involved
(46, 60).
EVOLUTION OF OVIPOSITION STRATEGIES
AND HOST ASSOCIATIONS
Oviposition Strategies and Egg Types
One of the most striking features of tachinids as a group is their wide diversity
of oviposition strategies and associated egg morphologies. These strategies have
been outlined several times in the literature, and the egg morphologies have been
subjected to a variety of classification schemes (14, 24, 150, 154, 164). Perhaps
the most significant division is between species that lay eggs on the host (direct
oviposition) (Figure 1) versus those that lay eggs away from the host (indirect
oviposition) (Table 2). The former type may be divided further depending on
whether eggs are laid externally or injected into the host and whether the eggs are
incubated (ovolarvipary) in a uterus and contain fully developed larvae when de-
posited or not (ovipary). Taxa with indirect oviposition can also be subdivided into
two major groups: ovolarviparous species, in which larvae hatch soon after eggs
are laid and either wait for passing hosts (e.g., many Tachininae) or actively search
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TABLE 2 Types of oviposition strategies in Tachinidae
Oviposition
strategy Egg type Taxa Fecundity
a
Indirect Ingested by host
(microtype)
Goniini, Blondeliini (e.g., Anisia,
Phasmophaga)
1000–6000 (2420)
Indirect Incubated Tachinini, Dexiini, Polideini
Few Exoristinae (e.g.,
Lixophaga)
500–8000 (1168)
Direct-external Incubated “Eryciini” (Exoristinae),
Blondeliini (most), Voriini,
Strongygastrini
30–600 (140)
Direct-external Unincubated
(planoconvex)
Phasiinae, Exoristiini,
Winthemiini, some Blondeliini,
Aplomya (Eryciini)
100–200
Direct-internal Incubated Blondeliini (e.g., Blondelia,
Eucelatoria), Dexiinae
(Palpostomatini)
65–250
Direct-internal Unincubated Phasiinae, Exoristiinae (e.g.,
Phorocera)
100–200
a
Fecundities are rough ranges taken from the literature (primarily derived from References 14, 24, and 154) with averages
in parentheses for some groups from Belshaw’s (14) compilation.
for hosts (e.g., Dexiini), and species possessing “microtype” eggs, in which ova are
ingested by hosts as they feed and hatch in the gut, and the emerging first-instar lar-
vaeburrow into the hemocoel (Figure 2). These diverse oviposition strategies have
evolved in concert with host-searching and attack strategies, changes in fecundity,
and the types of hosts attacked. As expected, given the probability of success-
ful parasitization, indirect egg-layers exhibit high fecundities of sometimes thou-
sands of eggs, whereas direct egg-layers tend to have more moderate fecundities
(Table 2).
Interestingly, the taxonomic diversity of tachinids is approximately evenly dis-
tributed across oviposition strategies. For example, at least 40% of Palearctic
species have indirect modes of oviposition (14), and the Tachinini (indirect “wait-
ers”), Dexiini (indirect “searchers”), and Goniini (microtype) are among the most
species-rich tribes of Tachinidae. Furthermore, these oviposition strategies may
have been gained or lost multiple times over tachinid evolution. Piercers for ex-
ample, which are present in about 7% of Palearctic tachinid species (14), have
evolved in three of the four subfamilies and at least four times in the Exoristinae
alone (137). This repeated evolution of piercing structures and consequent internal
oviposition may be associated with selection to minimize the likelihood that eggs
will be destroyed by the host or shed during host molting (53). Transitions from
unincubated (presumably ancestral) to incubated egg types may also have occurred
more than once, given the presence of both forms in Eryciini and Blondeliini of
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the Exoristinae, but the absence of a credible phylogeny of Tachinidae prevents
strong inferences concerning the evolution of egg type. Note that these categories
are not entirely distinct, with the incubation of a single egg at a time occurring in
some if not most species possessing unincubated macrotype eggs (65, 148). Even
the highly derived strategy of laying minute eggs that are inadvertently consumed
by the host appears to have evolved at least twice in different tribes [Goniini and
Blondeliini (Phasmophaga, Anisia)] (162) and possibly has been gained or lost
multiply in the Goniini (140).
Given that nearly one half of all tachinid species oviposit indirectly (37), these
strategies appear to have been important innovations in tachinid evolution. Be-
cause tachinids generally attack active life stages of their hosts and do not possess
paralytic poisons with which to subdue them, behavioral and morphological de-
fenses of hosts may present formidable barriers to oviposition. Host defenses such
as biting, thrashing, stinging hairs or spines, and gregariousness may have initially
encouraged the evolution of indirect oviposition strategies and promoted the diver-
sification of tachinid taxa possessing them. Furthermore, given the diurnal habits of
most species and the lack of specialized ovipositors (as in the Hymenoptera), many
concealed and/or nocturnal hosts must have been inaccessible to early tachinids.
The evolution of host-searching first instars that burrow through soil or into gal-
leries of concealed insects, of larvae that ambush nocturnally feeding caterpillars
on their host plants, and of microtype eggs that can be ingested by nocturnal or
well-defended hosts all served to expand the range of hosts that are vulnerable to
attack. These innovations may have opened extensive adaptive zones for tachinids
to colonize. Most microtype Goniini and many Tachininae, however, attack hosts
that are apparently accessible to direct oviposition (i.e., diurnal exophytic Lepi-
doptera). Thus, although indirect oviposition may have been frequently exploited
to allow the attack of inaccessible hosts, it may often be more profitably viewed
as a strategy to reduce search time, handling time, and potential injury associated
with oviposition (144).
HOST ASSOCIATIONS
Tachinids exploit a wide diversity of hosts belonging to many orders and families
of insects (and a few other arthropods). Aside from a few taxonomically coarse
associations of tachinid taxa with particular host orders and families, host asso-
ciations are evolutionarily labile within Tachinidae, often varying considerably
among congeneric species. Detailed host associations of tachinid taxa have been
summarized for most regions (8, 13, 26, 28, 55, 64, 131); therefore only some of
the general associations are summarized here (Figure 3). The strictest associations
between tachinid and host groups are the restriction of Phasiinae to heteropterous
hosts and Rutiliini to scarab hosts. Other broad associations include Scarabaeidae
as hosts of Dexiini, Lepidoptera as hosts for most Tachininae and Exoristinae (as
well as Voriini of Dexiinae), and Orthoptera as hosts for Ormiini (Figure 3). Even
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where these broad associations occur, however, there is often little phylogenetic
signal in host use at finer levels (140, 144). This phylogenetic lability of host as-
sociations, along with our poor phylogenetic understanding of Tachinidae, makes
it difficult to draw many conclusions concerning the evolution of host associations
in the family. The widespread use of Lepidoptera in Exoristinae, Tachininae, and
Dexiinae suggests that members of this order may have served as ancestral hosts
of tachinids. This inference cannot be corroborated through outgroup analysis be-
cause the sister group to the Tachinidae is unclear and parasitism of insects may be
a derived character of the family absent in early ancestors. An early shift in host use
from Lepidoptera to Heteroptera apparently occurred in Phasiinae, a seemingly
primitive lineage that has retained the ancestral habit of producing unincubated
eggs.
Most tachinids attack exophytic caterpillars or other larvae of holometabolous
insects that are ecologically and morphologically similar to caterpillars, such as
larval sawflies and chrysomelid beetles (35). The predominance of these insects
as hosts of tachinids may be explained by their external feeding habit, generally
weak physical defenses, taxonomic diversity, adequate size, and perhaps most im-
portantly, their specialized associations with plants. In general, the most diverse
clades of parasitoids including Tachinidae, Chalcidoidea, and Ichneumonoidea at-
tack primarily phytophagous insects, and the tritrophic interactions between plants,
phytophagous insects, and parasitoids may play a central role in both herbivore
and parasitoid diversification. The indirect effects of plants on parasitoids, via
their role in host location by parasitoids and their use as defenses against para-
sitoids by herbivores (e.g., sequestered secondary compounds), should select for
increased specialization and encourage diversification in parasitoids. Explicit con-
sideration of the tritrophic framework of host plants, herbivores, and tachinids is
central to understanding patterns of tachinid host use at both microevolutionary
and macroevolutionary scales.
HOST RANGE
The apparent lability of host use among most Tachinidae may be due to a gen-
eral lack of host-specific adaptations relating to host physiological defenses. Lar-
val tachinids are well known for their formation of respiratory funnels derived
from host defensive cells. Rather than evading or destroying host hematocytes
as do many hymenopteran parasitoids (145), tachinids often coopt them to form
“breathing tubes. These structures allow many tachinids to maintain direct contact
with atmospheric air via their posterior spiracles through either the host’s external
integument or major tracheal branches (24). The ability to capitalize on the im-
mune response by forming respiratory funnels may allow tachinids flexibility to
ecologically “explore” new hosts more easily, resulting in dynamic evolution and
diversification of host associations. This hypothesis is supported by the observa-
tion that tachinids that remain free in the hemocoel without forming a respiratory
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funnel exhibit significantly narrower host ranges than average for the family (14).
In addition, tachinids may be relatively tolerant of toxins actively or inadvertently
ingested by their hosts (46, 83), allowing greater evolutionary plasticity in host
range. This tolerance may be due to preadaptations associated with the ancestral
saprophagous habits of the Oestroidea (37), in which larvae faced with highly toxic
environments produced by bacteria and fungi accumulated adaptations to tolerate
these toxins. The apparent tolerance of tachinids to host physiological defenses
may be related also to the position of young larvae within the host. Many early
larval stages of tachinids embed themselves in specific tissues rather than float free
in the hemocoel (14), and at least one highly polyphagous species, Compsilura
concinnata, undergoes most of its larval development in the gut (i.e., between the
peritrophic membrane and gut wall) (70).
These arguments, that tachinids may overcome physiological defenses of the
host via the formation of respiratory funnels, through adaptations to toxic environ-
ments, or by “hiding” in specific tissues, have also been used to explain the wide
host ranges of many tachinid species (14). Some tachinids (e.g., C. concinnata,
Exorista mella, Lespesia aletiae) are unusually polyphagous, attacking dozens
of host species belonging to multiple families. Further, in analyzing host records
of Palearctic species, Eggleton & Gaston (37) and Belshaw (14) found a strong
correlation between the number of tachinid rearings and the number of hosts,
suggesting widespread polyphagy in Tachinidae. This has led to the general per-
ception that most or even all tachinids are polyphagous. However, this conclusion
may be misguided. First, parasitoid rearing data is riddled with misidentifications
of hosts and parasitoids (127). Second, generalists are reared far more often than
specialists, acquiring undue influence on regressions (e.g., it is likely that few
of the tachinid species for which no hosts are known are highly polyphagous).
Third, widespread polyphagous tachinid species may often consist of relatively
specialized, perhaps genetically differentiated, local populations. Finally, ow-
ing to the developmental permissiveness of tachinids, “mistakes” on alternative
hosts end up as observed rearings that obscure otherwise narrow host associa-
tions. Recent analyses of tachinid-host associations from a long-term intensive
caterpillar-rearing program in Costa Rica (more than 12,000 tachinid rearing
records; 74) indicate that most tachinid species are relatively specialized at a
local scale, attacking only one or a few host species, or a well-defined ecolog-
ical category of caterpillars (D.H. Janzen, personal communication). However,
these data also support the existence of a visible minority of highly polyphagous
species.
Tachinids possess several additional traits that may permit broad host ranges,
including external oviposition that does not expose the defenseless egg stage to host
immune defenses, rapid larval development, and oviposition on host-frequented
substrates. The notion that rapid larval development of tachinids may encour-
age polyphagy is supported by the finding that species exhibiting developmental
synchrony with hosts exhibit significantly narrower host ranges than those lack-
ing this synchrony (14). Another prediction that species with indirect oviposition
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should exhibit broader host ranges (because larvae with a low probability of con-
tacting a host should not be particularly selective) has not been borne out in
analyses of the literature (14) or in studies of particular tachinid-host commu-
nities (144). This is likely related to the observations that indirectly ovipositing
taxa deposit offspring on specific substrates (e.g., particular host plants) (120),
use fresh feeding damage by hosts as a cue for oviposition (91, 92), and may
visually or otherwise locate hosts and lay eggs in their vicinity (D.H. Janzen,
personal communication). Interestingly, polyphagous tachinids are widely dis-
persed among tachinid lineages, often occurring in genera that contain many spe-
cialized species (141). This indicates that host range is not strongly conserved
and not closely related to oviposition strategies or other major traits that define
clades within Tachinidae. It also suggests that tachinids are well suited for test-
ing the controversial hypothesis that host specialization promotes diversification
(37a).
Host Finding and Host Range
The previous discussion of evolutionary patterns of host associations and host
ranges proposes that, unlike many hymenopteran parasitoids (158), host associ-
ations of tachinids are not strongly limited by physiological suitability or host
defenses. Assuming that hosts are generally physiologically permissive for ta-
chinids and that even “generalist” tachinids use only a small fraction of potentially
available hosts, the obvious question arises: What then determines host ranges of
tachinids? One recurring observation concerning tachinid-host associations is that
the set of hosts tachinids attack may be more closely related to their ecology (e.g.,
habitat use) than to their phylogenetic affinities (14, 30, 37, 42). This observation
stems from the apparent ecological and evolutionary flexibility of tachinid-host
associations and is supported by strong effects of host plant species on parasitism
rates by tachinids in a variety of systems (43, 72, 82). It can be explained by
the use of relatively specific cues by tachinids to locate host habitats (e.g., host
plant volatiles) (119) and, once in the appropriate habitat, the use of relatively
indiscriminate cues to locate and/or select hosts (see Host Location and Selec-
tion, below). Thus, the processes of host location and selection that determine
proximate host use may ultimately shape broad-scale ecological and evolution-
ary patterns of host use. This suggests that it is the cues that determine which
hosts are attacked rather than the more conventional perspective that it is the host
that determines the cues used to locate it. In nature there likely exists a dynamic
interplay between behavioral mechanisms of host location that determine which
hosts are attacked and subsequent selection due to location efficiency and host-
related performance that shapes the evolution of these mechanisms. Although
the role of host location and selection behavior in shaping broader scale patterns
of host use has been relatively ignored historically, it has recently received in-
creased attention as a means of shaping host associations in phytophagous insects
(15).
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HOST LOCATION AND SELECTION
The mechanisms by which most tachinids locate and select hosts are not well
understood. Notably sparse is information about species in which the adults do
not contact the host directly. The information available on the small proportion
of species studied indicates that tachinids are capable of using a wide diversity
of olfactory, visual, auditory, and tactile-chemosensory cues to locate their hosts
(Table 3). It is clear from an examination of host location mechanisms that many
tachinids rely heavily on chemical cues derived from the host plants of their phy-
tophagous insect hosts or from interactions between hosts and host plants (91, 93,
120). These cues may serve to attract tachinids to the habitats or microhabitats oc-
cupied by their hosts, at which point more reliable close-range cues can be utilized
to detect the host or signs of the host’s presence. Close-range cues include odors
associated directly with the host, host secretions, or excretions (particularly frass),
and visual detection of hosts (Table 3). Several studies have shown that tachinid
oviposition behavior can be elicited in response to tactile-chemosensory cues as-
sociated with the host’s cuticle (19, 38), recently damaged leaves (92), and/or host
frass (123). In these cases females use chemosensors on their front tarsi (92, 123),
which may function similarly to the chemosensors on the long antennae of many
hymenopteran parasitoids. Such an explanation may account for the “drumming”
of tarsi on the host observed in Exorista species (138, 146).
Visual Cues
The use of visual cues is apparently integral to host location and selection for
many tachinids (94, 138, 139, 160, 165). Higher Diptera generally have well-
developed visual systems, particularly with regard to motion detection (20), and
this may have preadapted Tachinidae to rely on visual cues in locating and selecting
hosts. In some species motion of hosts or host-like objects appears to act as a
superstimulus, leading to indiscriminant oviposition, or at least ovipositor probing
of feathers, forceps, and even fingers (94, 137). This strong excitatory effect of
visual detection of host movement may play a role in generating patterns of host use
in tachinids that are related more to ecology and habitat use than to phylogenetic
affinities of hosts. Easily detectable cues such as volatile chemicals associated with
plants or plant damage may serve to attract female tachinids to particular habitats.
Once there, many tachinids may rely strongly on relatively indiscriminant visual
detection of host movement for host location and selection, leading to apparent
polyphagy within a habitat and perhaps rapid evolutionary changes in host use.
Learning
One phenomenon relating to host location and selection that has received little
attention in tachinids is learning. Given that many tachinid species attack mul-
tiple host species, and that several forms of learning have been demonstrated in
other insects including higher flies (107), it may be expected that sensitization or
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TABLE 3 A survey of mechanisms of host location and/or selection in Tachinidae
Tachinid species Subfamily (Tribe) Host Mode Source Cue Reference(s)
Compsilura
concinnata
Exoristinae
(Blondeliini)
Lymantria dispar
(Lymantriidae)
Visual Host Motion 160
Eucelatoria bryani Exoristinae
(Blondeliini)
Heliothis sp.
(Noctuidae)
Olfactory Host plant Damaged plant
volatile
86
Eucelatoria sp. Exoristinae
(Blondeliini)
Heliothis sp.
(Noctuidae)
Tactile
(chemosensory)
Host Cuticular extract 19
Eucelatoria sp. Exoristinae
(Blondeliini)
Heliothis sp.
(Noctuidae)
Olfactory Host ×
host plant
Plant volatiles
from herbivore?
97
Lixophaga diatraeae Exoristinae
(Blondeliini)
Diatrea saccharalis
(Crambidae)
Chemosensory Host Frass 123
Lixophaga diatraeae Exoristinae
(Blondeliini)
Diatrea saccharalis
(Crambidae)
Olfactory Host ×
host plant
Plant volatiles ×
host interaction
122
Drino bohemica Exoristinae (Eryciini) Neodiprion spp.
(Diprionidae)
Olfactory Host plant Plant volatiles 93
Drino bohemica Exoristinae (Eryciini) Neodiprion spp.
(Diprionidae)
Olfactory Host Plant/frass
volatiles?
93
Drino bohemica Exoristinae (Eryciini) Neodiprion lecontei
(Diprionidae)
Visual Host Motion 94
Drino inconspicua Exoristinae (Eryciini) Gilpinia hercyniae
(Diprionidae)
Visual tactile Host Motion +
“firmness”
31
Eucarcelia rutilla Exoristinae (Eryciini) Bupalus piniarius
(Geometridae)
and others
Olfactory Host plant Plant volatiles 62
Exorista japonica Exoristinae
(Blondeliini)
Mythimna separata
(Noctuidae)
Olfactory Frass Frass volatile 147
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Exorista japonica Exoristinae
(Blondeliini)
Mythimna separata
(Noctuidae)
Olfactory Host plant Damaged plant
volatile
76
Exorista japonica Exoristinae
(Blondeliini)
Mythimna separata
(Noctuidae)
Visual Host Motion 165
Exorista japonica Exoristinae
(Blondeliini)
Mythimna separata
(Noctuidae)
Visual Host Color, size 146
Exorista mella Exoristinae
(Blondeliini)
Grammia geneura
(Arctiidae)
Olfactory Host plant Damaged plant
volatile
138
Exorista mella Exoristinae
(Blondeliini)
Grammia geneura
(Arctiidae)
Visual Host Motion 138
Blepharipa pratensis Exoristinae (Goniini) Lymantria dispar
(Lymantriidae)
Tactile
(chemosensory)
Host plant Damaged plant
exudate
99
Cyzenis albicans Exoristinae (Goniini) Operophtera
brumata
(Geometridae)
Olfactory Host plant Plant volatile
(Borneol)
58, 119, 120
Leschenaultia exul Exoristinae (Goniini) Malacosoma
disstria
(Lasiocampidae)
Olfactory Host plant Damaged plant
volatile
91
Leschenaultia exul Exoristinae (Goniini) Malacosoma
disstria
(Lasiocampidae)
Olfactory Host Host frass 91
Leschenaultia exul Exoristinae (Goniini) Malacosoma
disstria
(Lasiocampidae)
Tactile
(chemosensory)
Host plant Damaged plant
exudate
92
Patelloa pachypyga Exoristinae (Goniini) Malacosoma
disstria
(Lasiocampidae)
Olfactory Host plant Damaged plant
volatile
91
(Continued)
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TABLE 3 (Continued)
Tachinid species Subfamily (Tribe) Host Mode Source Cue Reference(s)
Hemyda aurata Phasiinae
(Cylindromyini)
Podisus spp.
Euschistus spp.
(Pentatomidae)
Olfactory Host Male pheromone 2
Gymnoclytia
occidentalis
Phasiinae
(Gymnosomatini)
Euschistus
conspersus
(Pentatomidae)
Olfactory Host Male pheromone 79
Euclytia flava Phasiinae (Phasiini) Podisus spp.
Euschistus spp.
(Pentatomidae)
Olfactory Host Male pheromone 2
Trichopoda pennipes Phasiinae
(Trichopodini)
Nezara viridula
(Pentatomidae)
Olfactory Host Male pheromone 57
Linnaemyia
(Bonnetia) comta
Tachininae
(Ernestiini)
Agrotis ipsilon
(Noctuidae)
Olfactory/
(chemosensory)
Host Frass, vomit 124
Triarthria setipennis Tachininae
(Loewiini)
Forficula
auricularia
Olfactory Host Host
kairomones?
80
Homotrixia alleni Tachininae (Ormiini) Sciarasga quadrata
(Tettigoniidae)
Auditory Host Sexual calls 3, 4
Ormia ochracea Tachininae (Ormiini) Teleogryllus
oceanicus
(Gryllidae)
Auditory Host Sexual calls 21, 159
Therobia leonidei Tachininae (Ormiini) Poecilimon sp.
(Tettigoniidae)
Auditory Host Sexual calls 81
Archytas marmoratus Tachininae
(Tachinini)
Heliothis virescens
(Noctuidae)
Tactile/chemosensory Host Protein 98
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associative learning of host-associated cues is widespread in tachinids. Learning
of habitat cues associated with hosts could be partially responsible for plant-
specific patterns of parasitism by tachinids, and learning or reinforcement of host-
associated cues may result in locally restricted host associations. However, the
capacity to learn has been demonstrated for only two species, Drino bohemica
(95) and Exorista mella (139). Interestingly, in both cases the tachinids learned
to associate visual cues with hosts, reaffirming the importance of this modality in
host location/selection.
Host Sexual Signals as Host Location Cues
One striking mode of host location by tachinids that has attracted a great amount
of attention in recent years is phonotactic attraction to sexual calls of crickets and
other Orthoptera by tachinids in the tribe Ormiini (Tachininae) (21, 96, 159). The
relatively well-studied species Ormia ochracea searches for hosts at night using
an “ear” located between the forecoxae to detect and locate calling male crickets,
upon which eggs are laid (21, 116). Similar strategies are utilized by other species
to attack other nocturnal song-producing hosts such as katydids (Tettigoniidae) (3)
and mole crickets (Gryllotalpidae) (44). This mode of host location is particularly
interesting because it results in trade-offs for calling males, which attract both
potential mates and deadly parasitoids. Such conflicting forces of sexual and natural
selection may result in strong coevolutionary dynamics between ormiine tachinids
and their hosts (167).
A similar exploitation of sexual signals by tachinids is found in a number of
Phasiinae that attack Heteroptera (2, 57). These tachinids, such as Trichopoda
pennipes, utilize the volatile sexual pheromones of their heteropteran hosts for
host location via chemotaxis (57). In at least one case, Euclytia flava, the tachinid
species appears to consist of cryptic “pheromone races” that are differentially sen-
sitive to particular pheromone components associated with different host species
(even more sensitive than the hosts themselves) (2). As in the hosts of Ormi-
ini, conflicting selection pressures associated with mate and parasitoid attraction
may lead to coevolutionary “arms races” in which hosts are constantly selected
to produce sexual signals unattractive to tachinids but attractive to mates (“new
codes”) and tachinids are constantly selected for greater sensitivity to these signals
(“code-breakers”). Repeated cycles of these dynamics may facilitate speciation and
evolutionary diversification of both players. Dependence on host pheromones in
host location is probably widespread in the Phasiinae and may have been pivotal
in their evolutionary radiation on heteropteran hosts.
ECOLOGY OF TACHINID-HOST INTERACTIONS
The long history of tachinids in biological control programs attests to their impor-
tance as enemies of phytophagous pest insects (12, 50). Yet, tachinids’ roles as
enemies of native herbivores and their larger roles in the structure and dynamics
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of natural ecosystems have been largely uninvestigated. Recent data from several
large-scale caterpillar-rearing programs focusing on exophytic macrolepidoptera
have shown that mortality from tachinids is often equivalent and sometimes greater
than that due to hymenopteran parasitoids. For example, tachinids were responsible
for more than half of caterpillar mortality due to insect parasitoids in rearing studies
focused on a diversity of ecosystems including Southwestern United States desert-
savanna (143), Northeastern United States forests (128), Costa Rican tropical dry
forest (73), Costa Rican tropical wet forest (47), and Ecuadorian montane wet forest
(L.A. Dyer & H.F. Greeney, personal communication).
Ta chinid Community Ecology
As the field of parasitoid community ecology has developed over the past two
decades (61), the number of studies dealing with the structure and dynamics of
tachinid-host associations has dramatically increased (47, 82, 128, 143). This is
due primarily to a broader emphasis on ecological communities (rather than single
species) and to a growing realization of the importance of higher trophic levels
in shaping the ecology and evolution of insect communities. The goals of these
studies have been largely to understand how and why parasitism frequencies and
richness of parasitoid species vary among host species. Several relationships be-
tween host traits and tachinid parasitism or diversity have been documented, some
of which appear to be consistent across ecosystems. For example, analyses of large-
scale caterpillar-rearing programs by both Sheehan (128) and Stireman & Singer
(143) found that abundant, gregarious, and host plant generalist caterpillars were
attacked by significantly more tachinid species than their rare, specialist, and/or
solitary counterparts. Both studies suggested that this pattern is associated with the
process of host finding. Stireman & Singer (143) also found that hairy caterpillars
exhibited significantly larger tachinid assemblages than did smooth caterpillars.
This result, along with positive associations between tachinid parasitism and both
gregariousness and shelter-building among caterpillars, has been used as evidence
that enemy-free space (75) may be important in determining patterns of tachinid
host use (47, 143). That is, hosts that are well defended against predators may be
particularly suitable for tachinid parasitoids because in these hosts an immature
parasitoid is less likely to be devoured by a predator.
Ta chinid Population Ecology
Although the prominent insect population ecologist M.P. Hassell (59) developed
several of his influential ideas with a tachinid-host system (58), only recently
have other population ecology researchers become aware of the utility of tachinid-
host systems in understanding general ecological processes (23, 106, 109). This
usefulness is evident in a recent research program studying the spatial structure
of western tussock moth outbreaks (Orgyia vetusta) (85). Detailed work on this
system involving the tachinid Ta chinomyia similis has carefully elucidated how
strong dispersal and density-dependent host searching by this tachinid result in a
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patchy spatial structure of localized host outbreaks, dampening and weakening the
spread of host population irruptions (18, 84, 155). Given well-developed flying
abilities, most tachinids are likely excellent dispersers, suggesting that population
interactions exemplified by T. similis and its host may be widespread.
As discussed previously, many studies have demonstrated that parasitism by
tachinids is often highly dependent on habitat, particularly on the food plant of the
host (10, 82, 142, 160). Recent detailed ecological research on spatial patterns of
parasitism has also revealed that tachinids respond strongly to the spatial structure
of habitats or host plants (23, 32). A particularly nice example is the work of Roland
&Taylor (121). These authors showed that parasitism by three tachinid species
and a sarcophagid pupal parasitoid on the forest tent caterpillar (Malacosoma
disstria) responds strongly (and disparately) to forest structure, with larger bodied
parasitoids being more sensitive to forest structure and less likely to parasitize
hosts in small fragments. On the basis of these results, the authors inferred that
forest fragmentation could interfere with host population regulation by this tachinid
community. A recent study of the insect community associated with a bracket
fungus in old-growth forests also indicates a strong dependence of parasitism on
habitat structure (78). The primary parasitoid in this food chain, Phytomyptera
cingulata (as Elfia cingulata;Tachininae), declined in frequency with the age
of forest fragments and was completely absent from the oldest fragments (12 to
32 years). Because tachinids occupy higher trophic levels and may be relatively
sensitive to habitat structure and composition, they (and other parasitoids) may be
particularly well suited as indicators of ecosystem health.
Tritrophic Interactions
The frequent finding that tachinid parasitism varies strongly with habitat has im-
portant implications for the evolution and diversification of both tachinids and
their mostly plant-feeding hosts. There is a growing consensus among researchers
that to understand patterns of ecological specialization and evolutionary diversifi-
cation in phytophagous insects, one must consider not only their interactions with
their host plants but also tritrophic interactions involving natural enemies (16, 110,
152). Although much of the interaction between tachinids and plants may be via
the cues plants provide in host location (Table 3), recent studies have indicated
that tritrophic interactions may also take place between larval tachinids, hosts, and
host food plants. One interesting example is the interaction between the arctiid
caterpillar Platyprepia virginalis and the tachinid Thelaira americana,inwhich
the host often survives parasitism despite emergence of mature T. americana larvae
(39). Survival of the host, however, is strongly dependent on the food plant, with
parasitized larvae preferring the plant Conium maculatum, which increases their
chances of surviving parasitism (77). The work of Singer and colleagues (132–
134) on interactions between tachinid parasitoids and polyphagous arctiids shows
evidence of similar tritrophic interactions. In these studies, caterpillars exhibited
increased survival via lower parasitism rates when fed diets of noxious plants,
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which were poor for growth and survival in the absence of parasitoids. These re-
sults suggest that polyphagy in some insects may be maintained because some food
plants are more suitable for efficient growth (“good” plants) while others provide
benefits through protection against parasitoids such as tachinids (“nasty” plants)
(133). These results also suggest that at least some tachinid species are susceptible
to host plant toxins ingested by the host.
There has been a long and valuable history of applied and basic research on
tachinid-host associations since the early 1900s (7, 24, 54, 64), but only recently
has ecological research on tachinids been widely integrated into modern ecological
and evolutionary theory (13, 60, 143). Despite a recent flourish of basic studies
and the more extensive applied ecological research, our knowledge of the ecology
of most tachinid species is at best rudimentary. Currently, certain lines of inquiry
are hampered by practical issues such as the inability to breed most species in the
laboratory. On the other hand, this paucity of knowledge, the potential of tachinid-
host interactions as model systems in the field, and the important role of tachinids
as enemies of many crop and forest pests suggest that ecological research involving
tachinids offers both expansive opportunity and great reward.
CONCLUSIONS AND FUTURE DIRECTIONS
Given the many constraints of a review article, this review provides only a cursory
overview of tachinid biology. Many interesting and active areas of research have
been mentioned only in passing or have been omitted altogether. Perhaps most
noticeable is the sparse coverage of biological control involving tachinids and
tachinid-host interactions in managed agricultural systems. Our avoidance of these
issues is not due to a lack of perceived importance but rather to the realization that
we cannot possibly do justice to them in this limited space, and they have been
summarized in various articles (50). However, we hope to have conveyed some
appreciation of tachinid biology and the many ways in which the study of this
diverse group can provide insight into larger issues of evolution, ecology, and
behavioral ecology. Furthermore, we hope to have impressed upon students and
researchers the fragmentary extent of our knowledge of tachinids and the many
interesting questions and areas of research that have yet to be fully explored. The
following are a few of the promising future directions of research on the Tachinidae:
Molecular ecology of tachinids. Little research has been conducted exam-
ining the genetic structure of tachinid populations and how this may vary
according to geography and host use. We know of only a single study (126)
that has examined population genetic structure in tachinids, and it focused on
an introduced species in its introduced range. Evidence of cryptic pheromone
races in Phasiinae (2) suggests that phylogeography and population genetic
techniques could provide great insight into the evolutionary diversification
and host relationships of Tachinidae.
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Phylogenetic/comparative studies. The evolutionary relationships of Tachi-
nidae remain largely unresolved, as is our understanding of the evolution of
morphological, behavioral, and ecological traits in the family. Modern phy-
logenetic analyses, as well as basic taxonomic studies, are sorely needed and
are likely to provide fundamental insights into the evolution of life-history
strategies and host associations and their relationship to macroevolutionary
patterns of diversity.
Tritrophic interactions. Initial research on tritrophic interactions involv-
ing tachinids, herbivorous hosts, and plants has produced some exciting
results (82, 132, 133). These interactions are paramount in determining
the ecological structure and dynamics of tachinid-host interactions, and
given the significant roles of phytophagous insects in terrestrial ecosys-
tems, they may frequently have broader community- and ecosystem-level
impacts.
ACKNOWLEDGMENTS
We would like to acknowledge Mike Singer and two anonymous reviewers for
providing valuable comments on this manuscript. JOS would also like to thank
Liz Bernays, Don Feener, Molly Hunter, Dan Janzen, David Maddison, Nancy
Moran, and Bob Smith for encouraging his studies of and interest in Tachinidae.
The Annual Review of Entomology is online at http://ento.annualreviews.org
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by Wright State University - Library on 03/12/06. For personal use only.
Figure 1 A Winthemia species (Exorisinae: Winthemiini)
depositing macrotype (unincubated) eggs on its sphingid host
(photo courtesy of Robert W. Mitchell and Paul H. Arnaud, Jr.).
TACHINIDAE C-1
Figure 2 Belvosia bifasciata (Goniini), which deposits micro-
type eggs that are ingested by the hosts on their food plants
(photo courtesy of J.O. Stireman, III).
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C-2 STIREMAN
O’HARA
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Figure 3 Host associations of the major subfamilies of Tachinidae and their included
tribes. On the right are Holometabolous host groups; on the left are all other hosts. Box
heights indicate relative species diversity of the four subfamilies (154). Tribal names in
bold indicate major tribes in each subfamily (approximately >30 species). The width of the
colored wedges indicates the rough proportion of use of different host groups by each
tachinid subfamily as based on published records (8, 13, 26, 28, 55, 64).
HI-RES-EN51-22-Stire.qxd 11/23/05 4:46 PM Page 2
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P1: JRX
November 2, 2005 13:47 Annual Reviews AR263-FM
Annual Review of Entomology
Volume 51, 2006
CONTENTS
SIGNALING AND FUNCTION OF INSULIN-LIKE PEPTIDES IN INSECTS,
Qi Wu and Mark R. Brown 1
PROSTAGLANDINS AND OTHER EICOSANOIDS IN INSECTS:BIOLOGICAL
SIGNIFICANCE, David Stanley 25
BOTANICAL INSECTICIDES,DETERRENTS, AND REPELLENTS IN
MODERN AGRICULTURE AND AN INCREASINGLY REGULATED
WORLD, Murray B. Isman 45
INVASION BIOLOGY OF THRIPS, Joseph G. Morse and Mark S. Hoddle 67
INSECT VECTORS OF PHYTOPLASMAS, Phyllis G. Weintraub
and LeAnn Beanland 91
INSECT ODOR AND TASTE RECEPTORS, Elissa A. Hallem, Anupama
Dahanukar, and John R. Carlson 113
INSECT BIODIVERSITY OF BOREAL PEAT BOGS, Karel Spitzer
and Hugh V. Danks 137
PLANT CHEMISTRY AND NATURAL ENEMY FITNESS:EFFECTS ON
HERBIVORE AND NATURAL ENEMY INTERACTIONS, Paul J. Ode 163
APPARENT COMPETITION,QUANTITATIVE FOOD WEBS, AND THE
STRUCTURE OF PHYTOPHAGOUS INSECT COMMUNITIES,
F. J. Frank van Veen, Rebecca J. Morris, and H. Charles J. Godfray 187
STRUCTURE OF THE MUSHROOM BODIES OF THE INSECT BRAIN,
Susan E. Fahrbach 209
EVOLUTION OF DEVELOPMENTAL STRATEGIES IN PARASITIC
HYMENOPTERA, Francesco Pennacchio and Michael R. Strand 233
DOPA DECARBOXYLASE:AMODEL GENE-ENZYME SYSTEM FOR
STUDYING DEVELOPMENT,BEHAVIOR, AND SYSTEMATICS,
Ross B. Hodgetts and Sandra L. O’Keefe 259
CONCEPTS AND APPLICATIONS OF TRAP CROPPING IN PEST
MANAGEMENT, A.M. Shelton and F.R. Badenes-Perez 285
HOST PLANT SELECTION BY APHIDS:BEHAVIORAL,EVOLUTIONARY,
AND APPLIED PERSPECTIVES, Glen Powell, Colin R. Tosh,
and Jim Hardie 309
vii
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November 2, 2005 13:47 Annual Reviews AR263-FM
viii CONTENTS
BIZARRE INTERACTIONS AND ENDGAMES:ENTOMOPATHOGENIC
FUNGI AND THEIR ARTHROPOD HOSTS, H.E. Roy,
D.C. Steinkraus, J. Eilenberg, A.E. Hajek, and J.K. Pell 331
CURRENT TRENDS IN QUARANTINE ENTOMOLOGY, Peter A. Follett
and Lisa G. Neven 359
THE ECOLOGICAL SIGNIFICANCE OF TALLGRASS PRAIRIE
ARTHROPODS, Matt R. Whiles and Ralph E. Charlton 387
MATING SYSTEMS OF BLOOD-FEEDING FLIES, Boaz Yuval 413
CANNIBALISM,FOOD LIMITATION,INTRASPECIFIC COMPETITION, AND
THE
REGULATION OF SPIDER POPULATIONS, David H. Wise 441
BIOGEOGRAPHIC AREAS AND TRANSITION ZONES OF LATIN AMERICA
AND THE
CARIBBEAN ISLANDS BASED ON PANBIOGEOGRAPHIC AND
CLADISTIC ANALYSES OF THE ENTOMOFAUNA, Juan J. Morrone 467
DEVELOPMENTS IN AQUATIC INSECT BIOMONITORING:A
C
OMPARATIVE ANALYSIS OF RECENT APPROACHES, N
´
uria Bonada,
Narc
´
ıs Prat, Vincent H. Resh, and Bernhard Statzner 495
TACHINIDAE:EVOLUTION,BEHAVIOR, AND ECOLOGY,
John O. Stireman, III, James E. O’Hara, and D. Monty Wood 525
TICK PHEROMONES AND THEIR USE IN TICK CONTROL,
Daniel E. Sonenshine 557
CONFLICT RESOLUTION IN INSECT SOCIETIES, Francis L.W. Ratnieks,
Kevin R. Foster, and Tom Wenseleers 581
ASSESSING RISKS OF RELEASING EXOTIC BIOLOGICAL CONTROL
AGENTS OF ARTHROPOD PESTS, J.C. van Lenteren, J. Bale, F. Bigler,
H.M.T. Hokkanen, and A.J.M. Loomans 609
DEFECATION BEHAVIOR AND ECOLOGY OF INSECTS, Martha R. Weiss 635
PLANT-MEDIATED INTERACTIONS BETWEEN PATHOGENIC
MICROORGANISMS AND HERBIVOROUS ARTHROPODS,
Michael J. Stout, Jennifer S. Thaler, and Bart P.H.J. Thomma 663
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Annu. Rev. Entomol. 2006.51:525-555. Downloaded from arjournals.annualreviews.org
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... Antennae of tachinid flies are bestrewn with various types of sensilla that allow them to detect environmental signals to accurately locate hosts, mating partners, oviposition sites, and food (Rahal et al., 1996;Zhang et al., 2012b;Liu et al., 2013;Roh et al., 2020). The knowledge available indicates that tachinids mostly rely on chemical cues from infested host plants or from host and host plant interactions (Roth et al., 1982;Kainoh et al., 1999;Stireman et al., 2006) and, once in close proximity, close range chemical cues, such as host odors, secretions or excretions, can be vitally important, in addition to visual contact (Stireman et al., 2006). Previous studies of antennal sensilla of phytophagous, scatophagous, saprophagous and predaceous dipteran species have already revealed some taxonomic value, as well as phylogenetic and evolutionary trends (Ross, 1992;Sukontason et al., 2004;Liu et al., 2013Liu et al., , 2016Zhang et al., 2012aZhang et al., , b, 2013aZhang et al., , b, 2016Wang et al., 2012Wang et al., , 2014a. ...
... Antennae of tachinid flies are bestrewn with various types of sensilla that allow them to detect environmental signals to accurately locate hosts, mating partners, oviposition sites, and food (Rahal et al., 1996;Zhang et al., 2012b;Liu et al., 2013;Roh et al., 2020). The knowledge available indicates that tachinids mostly rely on chemical cues from infested host plants or from host and host plant interactions (Roth et al., 1982;Kainoh et al., 1999;Stireman et al., 2006) and, once in close proximity, close range chemical cues, such as host odors, secretions or excretions, can be vitally important, in addition to visual contact (Stireman et al., 2006). Previous studies of antennal sensilla of phytophagous, scatophagous, saprophagous and predaceous dipteran species have already revealed some taxonomic value, as well as phylogenetic and evolutionary trends (Ross, 1992;Sukontason et al., 2004;Liu et al., 2013Liu et al., , 2016Zhang et al., 2012aZhang et al., , b, 2013aZhang et al., , b, 2016Wang et al., 2012Wang et al., , 2014a. ...
Article
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Tachinidae are one of the most diverse clades of Diptera. All tachinids are parasitoids of insects and other arthropods, and thus are considered an important source of biological pest control. Antennae are the most important olfactory organs of Tachinidae playing key roles in their lives, especially in locating hosts, and details of antennal ultrastructure could provide useful features for phylogenetic studies and understanding their adaptive evolution. Despite the ecological and evolutionary importance of antennae, the current knowledge of antennal ultrastructure is scarce for Tachinidae. Our study examined antennal sensilla of thirteen species belonging to thirteen genera within eleven tribes of all the four subfamilies (Phasiinae, Dexiinae, Tachininae, and Exoristinae): Beskia aelops Walker, Trichodura sp., Voria ruralis (Fallén), Zelia sp., Cylindromyia carinata Townsend, Phasia xenos Townsend, Neomintho sp., Genea australis (Townsend), Copecrypta sp., Hystricia sp., Belvosia sp., Leschenaultia sp., and Winthemia pinguis (Fabricius). Types, length and distribution of antennal sensilla were investigated via scanning electron microscopy (SEM). Our comparative analysis summarized 29 variable characters and we evaluated their phylogenetic signal for subfamilial, tribal and generic/specific levels, showing that antennal ultrastructure could be a reliable source of characters for phylogenetic analysis. Our findings demonstrate the remarkable diversity of the antennal ultrastructure of Tachinidae.
... Tachinids are important dipteran biological control agents of phytophagous insects (Grenier 1988;Stireman et al. 2006). They are endoparasitoids of a variety of insects, the majority of which are lepidopteran larvae. ...
Article
Tryphera lugubris (Meigen, 1824) (Diptera: Tachinidae) was reared from larvae of Arctia festiva (Hufnagel, 1766) (Lepidoptera: Erebidae) feeding on yellow starthistle [Centaurea solstitialis L. (Asteraceae)] plants in Karacadag Mountain of Diyarbakr, Turkey. Arctia festiva was recorded for the first time as host of this parasitoid. Additionally, T. lugubris was recorded for the first time from Turkey. Some information on the host-parasitoid couple, and description of the parasitoid species, is also provided.
... These findings demonstrated that different host tissues exhibit diverse responses to tachinid parasitoids. Generally, the tachinid fly lays eggs on the host integument or food plant, then the hatched larvae invade from host integument or intestine into the hemocoel and build respiration funnels, the developing tachinid larvae are directly immersed in the hemolymph and contact with host hemocytes and fat body [16]. Therefore, tachinid parasitization should have profound effects on the physiology of host integument, hemocytes and fat body. ...
Article
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The dipteran tachinid parasitoids are important biocontrol agents, and they must survive the harsh environment and rely on the resources of the host insect to complete their larval stage. We have previously demonstrated that the parasitism by the tachinid parasitoid Exorista japonica, a pest of the silkworm, causes pupation defects in Bombyx mori. However, the underlying mechanism is not fully understood. Here, we performed transcriptome analysis of the fat body of B. mori parasitized by E. japonica. We identified 1361 differentially expressed genes, with 394 genes up-regulated and 967 genes down-regulated. The up-regulated genes were mainly associated with immune response, endocrine system and signal transduction, whereas the genes related to basal metabolism, including energy metabolism, transport and catabolism, lipid metabolism, amino acid metabolism and carbohydrate metabolism were down-regulated, indicating that the host appeared to be in poor nutritional status but active in immune response. Moreover, by time-course gene expression analysis we found that genes related to amino acid synthesis, protein degradation and lipid metabolism in B. mori at later parasitization stages were inhibited. Antimicrobial peptides including Cecropin A, Gloverin and Moricin, and an immulectin, CTL11, were induced. These results indicate that the tachinid parasitoid perturbs the basal metabolism and induces the energetically costly immunity of the host, and thus leading to incomplete larval–pupal ecdysis of the host. This study provided insights into how tachinid parasitoids modify host basal metabolism and immune response for the benefit of developing parasitoid larvae.
Chapter
In the laboratory, insects have demonstrated many times that they can evolve resistance to pathogens, parasitoids, and nematodes. However, a few cases of field-evolved resistance have been observed. Resistance can involve changes in behavior to avoid parasites, or it can occur through physiological mechanisms in the host’s body. Integrated pest management is important for delaying resistance in pests to biological control agents.
Article
Parasitoids are significant ecological elements of terrestrial food webs and have evolved within seven insect orders. Interestingly, however, associations with spiders as hosts have evolved only in two insect orders, Diptera and Hymenoptera. Here, we summarize various aspects of host utilization by dipteran flies with an emphasis on associations with spiders. Our synthesis reveals that spider flies (family Acroceridae) have evolved a unique life strategy among all the parasitoid taxa associated with spiders, in which koinobiont small-headed flies utilize an indirect oviposition strategy. This indirect oviposition in spider flies is inherited from Nemestrinimorpha ancestors which appeared in the Late Triassic and is characterized by the evolution of planidial larvae. Further, we discuss the advantages and disadvantages of indirect oviposition in spider flies. On the one hand, indirect oviposition allows the fly to avoid contact/wrestling with spider hosts. On the other hand, larval survival is low because the planidium must actively seek out and infect a suitable host individually. The risk of failure to find a suitable spider host is offset by the fly’s extremely high fecundity.
Article
Dipteran endoparasitoids avoid host immune response; however, antidefense components from the Dipterans are unknown. Infestation of commercial silkworm Bombyx mori Linnaeus (Lepidoptera: Bombycidae) by endoparasitoid Exorista bombycis Louis (Diptera: Tachinidae) induced immune reactions, cytotoxicity, granulation, degranulation, and augmented release of cytotoxic marker enzyme lactate dehydrogenase (LDH), and degranulation-mediator enzyme β-hexosaminidase in hemocytes. In this study, by reverse phase high-performance liquid chromatography, fractions of E. bombycis larval tissue protein with antihemocytic activity are separated. From the fraction, peptides of hemocyte aggregation inhibitor protein (HAIP) and pyridoxamine phosphate oxidase (PNPO) are identified by mass spectrometry. Interacting partners of HAIP and PNPO are retrieved that further enhance the virulence of the parasitoid. PNPO and HAIP genes showed a four- to seven fold increase in expression in the integument of the parasitoid larva. Together, the dipteran endoparasitoid E. bombycis exploit antihemocyte activity to inhibit host defense reactions in addition to defense evasion contemplated.
Chapter
Dipteran parasitoids (especially Tachinidae, but also Sarcophagidae, Phoridae, Cryptochaetidae, and Bombyliidae) comprise a number of species of interest for applied biological control and, as a consequence, mass production. Although they are underestimated and often forgotten in biocontrol strategies, several studies concerning their rearing technology have been carried out. The purpose of this chapter is to review the work done on dipteran parasitoids and bring this group of insects to light. Some examples of tachinid, phorid, and other dipteran parasitoids implicated in biological control are presented in the first section. Subsequently, the most important aspects of their biology relevant for rearing are described. In vivo and in vitro rearing techniques are considered in another section from different points of view, such as host type (natural vs alternative) and age, infestation mode, abiotic conditions, parasitoid nutritional needs, and continuous in vitro culture. Adult maintenance, quality control, storage and shipment procedures are also discussed, as well as sterilization and antimicrobial agents for diets/media. Finally, some perspectives are presented with the aim of stimulating new ideas for research efforts on the mass culturing of dipteran parasitoids.
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The aim of the research is to study the degree of infestation of female ants of the genus Lasius with the Tachinid flies Strongygaster globula. The study was performed in the town of Kungur (Perm Province, Russia). Overwintered queens of L. niger and L. flavus were collected in the amount of fifteen pieces of each species for four years in the spring. All this was placed in test tubes and kept for two months at a temperature of 25°C. Only queens of L. niger were infested, while all L. flavus queens bred. In 2018, out of fifteen L. niger queens caught, six individuals were infested (40%), in 2019 – nine individuals (60%), in 2020 – twelve (80%), and in 2021 – seven individuals (47%). In general, a high degree of infestation of L. niger queens with the Tahinid flies S. globula is noted in Kungur.
Article
This study was conducted between 2016-2020 to investigate the Tachinidae (Diptera) fauna of Manisa Province of Türkiye. For this purpose, Tachinidae samples were collected from the cultural and natural areas of five districts (Salihli, Sarıgöl, Selendi, Soma and Şehzadeler) selected to represent the province. Thirty-six species were determined and identified. These were four genera and five species in the subfamily Exoristinae, five genera and eight species in the subfamily Tachininae, three genera and four species in the subfamily Dexiinae, nine genera and 19 species in the subfamily Phasiinae. Among these, Estheria cristata (Meigen, 1826), Cistogaster globosa (Fabricius, 1775) and Cylindromyia gemma (Richter, 1972) (Diptera: Tachinidae) were recorded for the first time in Türkiye. The distributions and hosts in Türkiye of the identified species are given. In addition, the definitions of the species determined as new records for Türkiye are also included. This study is the first detailed study on the family Tachinidae in Manisa Province.
Article
Although they act as biocontrol agents, Tachinid parasitoids attack economically beneficial insects, inviting the adoption of control measures against them. The uzi fly, Exorista sorbillans, infests silkworms incurring heavy loss. It is difficult to control such parasitoids as the larval stage is endoparasitic, and insecticides cannot reach them without subjecting the silkworms to potential risks. We selected the leaves of Ocimum gratissimum L. for testing their toxicity potential against E. sorboillans because of its low selective toxicity to Antheraea assamensis Helfer larvae. Assay for adulticidal efficacy of the leaf extracts showed the petroleum ether extract to be the most effective. But the essential oil (LC50 of 0.42%) was even more effective. GC-MS analysis of the oil revealed the presence of twenty-seven compounds with a high percentage of thymol (26.17%), indicating the plant oil as thymol rich chemotype. Thymol was the dominant constituent in the active fraction. The oil and constituents caused rapid death on topical application, indicating a higher penetration rate. We propose the exploration of the essential oil and its constituents as a sustainable solution for controlling E. sorbillans infestation of silkworms in the future.
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Sixty-five specimens representing 49 species in 37 genera and 12, possibly 13, families of brachycerous Diptera are described in-detail. Some genera are family incertae sedis. They are preserved in Cretaceous ambers from the following areas and ages (abbreviations after each are used to designate the following origins of the ambers): Manitoba and Alberta, Canada (C) (Campanian); central, New Jersey (NJ) (Turonian); and Lebanon (L) (Neocomian). All taxa described are new species and most genera are described as new, except where noted. The new taxa and their origins are the following: Tethepomyia thauma (NJ), an extremely apomorphic fly of probable nematocerous affinities. In RHAGIONIDAE: Paleochrysophilus hirsutus (L), Jersambromyia borodini (NJ), Mesobolbomyia acrai (L); and four additional genera (3 L, 1 NJ) that are described and illustrated but not named because of incomplete preservation. STRATIOMYIDAE: it new specimen of Cretaceogaster pygmaeus Teskey (C) is reported, showing newly observed structures that confirm its extremely primitive position in the family; in addition, in NJ amber an additional primitive genus is described but not named, with affinities in the Pachygastrinae, Chiromyzinae, or Beridinae. HILARIMORPHIDAE: Hilarimorphites superba, H. yeatesi, and H. longimedia, all in NJ amber, and the only fossil hilarimorphids. SCENOPINIDAE(?): Proratites simplex (NJ), probably a primitive (proratine) scenopinid, which would be the only Mesozoic fossil of the family. ASILIDAE: an incomplete, unnamed specimen in NJ amber, which is one of only two Cretaceous records, The most diverse and numerous brachycerans in Cretaceous ambers-are in the EMPIDOIDEA, With new taxa as follows. EMPIDINAE: Turonempis styx (NJ), Emplita casei (NJ). ATELESTINAE: Atelestites senectus (L). NEMEDINA GENUS GROUP: Cretodromia glaesa (C); Nemedromia campania (C), N, telescopica (C), N. turonia (NJ); Neoturanius asymmetrus (NJ), N. cretatus (NJ), and N, vetus (NJ, possibly also C); Phaetempis lebanensis (L), which is possibly a very plesiomorphic member of this group. The Nemedina group today is represented by a single extant species from Hungary. TACNYDROMIINAE: Cretoplatypalpus americanus (C), with Cretoplatypalpus Kovalev previously known from a species in Cenomanian amber from northern Siberia; and Mesoplatypalpus carpenteri (C). TRICHOPEZINAE: Apalocnemis canadambris (C), which is the only species studied here belonging to an extant genus, Apalocnemis Philippi (previously known only from extant species widespread in distribution). MICROPHORINAE: Microphorites similis and M. oculeus (L), two additional species of the extinct genus Microphorites Hennig, known only from Lebanese amber; Avenaphora hispida (L); Cretomicrophorus novemundus (NJ), the second species in the extinct genus Cretomicrophorus Negrobov, originally known from Cretaceous amber of Siberia; Archichrysotus incompletus (NJ) and A. manitobus (C), the genus also previously known from Siberian amber. DOLICHOPODIDAE: Sympycnites primaevus (L), which is the oldest definitive dolichopodid. Three new species are described in an unusual new genus, Chimeromyia, known only from Lebanese amber: C. intriguea, C. acuta, and C. reducta. Chimeromyia possesses features of Empidoidea and Cyclorrhapha. The few Cyclorrhapha in Cretaceous ambers are all very plesiomorphic. PLATYPEZIDAE: Electrosania cretica (NJ), the most plesiomorphic known platypezid. Lebambromyia acrai (L), formally unplaced to family, is a plesiomorphic phoroid closely resembling IRONOMYIIDAE (with one living species in Australia and Tasmania, and one extinct species previously described in Canadian amber). LONCHOPTERIDAE: Lonchopterites prisca (L) and Lonchopteromorpha asetocella (L), the only definitive fossils of this small, extant family, SCIADOCERIDAE: Archiphora pria (NJ); and Archisciada lebanensis (L), the oldest fossil of the family and perhaps the most plesiomorphic phoroid. In addition, two new species are described in the Mesozoic genus Prioriphora McAlpine and Martin, P. luzzii and P. casei (both NJ). This is the best represented brachyceran genus in the Cretaceous, although it might be a paraphyletic taxon. Three cyclorrhaphan larvae of uncertain family identities are described, all in NJ amber; one appears similar to Sciadoceridae. Phylogenetic significance of most of these fossils are discussed, as are certain characters of traditional importance in the higher classification of Brachycera, such as the number of aristal articles. The fossils are placed onto cladograms of the lower Brachycera, the Empidoidea, and basal Cyclorrhapha, and a chronology is proposed of the origins of brachyceran families. The Brachycera apparently originated in the Lower Jurassic, with the Asiloidea not diversifying until the Lower Cretaceous. The Eremoneura (Empidoidea + Cyclorrhapha), as expected, show later diversification, with subfamily-level radiations of empidoids in the Lower to mid-Cretaceous, and the most plesiomorphic families of Cyclorrhapha (e.g., Platypezoidea, Phoroidea, Lonchopteridae) appearing in the Lower to mid-Cretaceous. Origins and radiations of the Schizophora almost certainly are of more recent origin, in the mid to latest Cretaceous and especially the Cenozoic. The diversity and detailed preservation of these fossils contribute exceptional insight into the early evolution of the Brachycera and the Eremoneura in particular.
Article
Signals used to attract mates are often conspicuous to predators and parasites, and their evolution via sexual selection is expected to be opposed by viability selection. Many secondary sexual traits may represent a compromise between attractiveness and avoidance of detection. Although such signal exploitation appears to be widespread, most examples come from species that use acoustic or olfactory mating signals, and relatively few cases of visual signal exploitation can be substantiated. Because males are usually the signaling sex, they are more at risk from predators or parasitoids that locate prey or hosts by sexual signals; this differential selection on the two sexes can affect the intensity of sexual selection on male ornamental traits. The notable exception to male signaling and female attraction occurs in pheromone-producing insects, particularly lepidopterans, which show an opposite pattern of female odor production. Exploitation of such sex pheromones is relatively rare. We discuss reasons for the reversal in sex roles in these species and its implications for signal exploitation. Changes in signals that appear to be adaptations to avoid predation include the use of different signal modalities, changes in signaling behavior, loss of signals, and alteration of signal characteristics such as pitch. Selection pressure from signal exploiters could lead to the production of a novel signal and thus facilitate speciation. Relatively little work has been done on adaptations on the part of the exploiting species, but such adaptations could indirectly influence the mating system of the predator or parasitoid. Signal exploitation is also expected to be a fruitful source of examples of coevolution. Finally, plants emit attractants analogous to secondary sex characters in animals, and may also be vulnerable to signal exploitation.
Article
Condensed tannin is generally considered an example of a quantitative plant allelochemical defense, and catalpol an example of a qualitative chemical defense. The effects of these compounds on the growth and survival of a tachinid parasitoid, Compsilura concinnata (Meigen), reared in the gypsy moth, Lymantria dispar (L.), were compared. Each chemical was incorporated into synthetic diets in a range of ecologically relevant doses and fed to host larvae. Larvae were fed in each of two ways: immediately after parasitization (one day after fourth instar molt), and from egg hatch onward. Growth and survival of unparasitized gypsy moth larvae on test diets were also monitored. No significant effect of either catalpol or condensed tannin on C. concinnata growth or puparial survival was observed. Tannin did lengthen development time of unparasitized host larvae from fourth stadium onward, and lowered pupal weights of larvae fed tannin from egg hatch onward. Catalpol had no significant impact on overall gypsy moth larval development, indicating that this insect is able to compensate for the reduction in weight gain reported to be caused by catalpol in younger larvae. Mortality in all experiments was insignificant. It appears that these phytochemicals are more similar in their effects on the parasitoid than was predicted based on their roles as toxins and digestibility-reducers in herbivores. The data also suggest that generalist tachinid parasitoids such as C. concinnata may be more tolerant of allelochemicals in their host's diet, than their hymenopteran counterparts.