461
Conopidae (thickheaded flies), Pyrgotidae (light flies), Cryptochaetidae (scale parasite flies), Chloropidae (frit flies), Anthomyiidae (root maggots), Muscidae (house
flies), Calliphoridae (carrion flies), Rhinophoridae (woodlouse flies), Sarcophagidae
(flesh flies) and Tachinidae (tachina flies). The second most common route to parasitoidism in Diptera is through predation, which has been documented seven times
and frequently has been associated with prey items occurring in or on top of the soil.
This route has been inferred for Cecidomyiidae (gall midges), the common ancestor
of Nemestrinidae + Acroceridae (tanglevein flies and spider flies), Bombyliidae
(bee flies) that are also associated with cleptoparasitoidism, Asilidae (robber flies),
Empididae (dance flies), Sciomyzidae (snail-killing flies) and Phacomyiidae (marsh
flies). For dipteran parasitoids, it appears that ants are the most common host group
(Quevillon and Hughes 2018).
A family-level phylogenetic tree of Diptera indicates that ectoparasitoidism originated 10 times, occurring sporadically throughout the phylogeny, whereas endoparasitoidism originated 17 times, largely confined to the Eremoneura (Wiegmann
et al. 2011). This asymmetry in distribution of the two major parasitoid types is
attributable to two major morphological features, the piercing ovipositor of some
Eremoneura (Yeates and Wiegmann 1999), and compensatory behavioral changes
for host seeking in other Eremoneura that lack a penetrative ovipositor (Feener and
Brown 1997). Behavioral features promoting parasitoidization that substitute for a
rigid, puncturing ovipositor include host consumption of parasitoid eggs that hatch
in the gut and invade internal organs (Stireman III et al. 2006), and larvae that
aggressively penetrate the host integument (Feener and Brown 1997; Stireman III
et al. 2006). These features allow Eremoneura to attack and penetrate hosts that
normally would be available only to apocritan Hymenoptera with extensive ovipositor modifications such as lengthening (Eggleton and Belshaw 1992; Feener and
Brown 1997). Most Diptera lack a prolonged, robust ovipositor for penetrating long
distances through indurated tissues as in Hymenoptera, and instead have a flexible,
telescopic ovipositor that is extended by intersegmental membranes, rendering it
inefficient for placing parasitoid eggs deep into host tissue (Feener and Brown
1997). Such ovipositor design restricts many dipteran parasitoid-bearing lineages to
exposed hosts and a preference for ectoparasitoidism over endoparasitoidism, the
latter of which only occasionally occurs across Diptera phylogeny (Eggleton and
Belshaw 1993; Wiegmann et al. 2011). Several derived eremoneuran clades—particularly well developed in Tachinidae (tachina flies), Conopidae, Pipunculidae and
Phoridae (scuttle flies)—have re-evolved stiffened, piercing, albeit undirected, ovipositors with a sclerotized terminus capable of penetrating their hosts (Feener and
Brown 1997; Poinar Jr 2013), allowing for endoparasitoidism. For this reason, there
is the dominance of endoparasitoidism over ectoparasoidism particularly among
Eremoneura (Table 11.1) (Wiegmann et al. 2011). Nevertheless, dipteran parasitoids have never developed capabilities for attacking wood-boring larvae separated
from a bark surface by several centimeters of wood; nor have they been engaged in
penetration of thick, hardened tissues such as galls (Eggleton and Belshaw 1993;
Quicke 1997). However, a substitute for reaching larvae via an ovipositor is hearing
convergence in cricket hosts and their tachina fly parasitoids (Robert et al. 1992).
11 The History of Insect Parasitism and the Mid-Mesozoic Parasitoid Revolution
Conopidae (thickheaded flies), Pyrgotidae (light flies), Cryptochaetidae (scale parasite flies), Chloropidae (frit flies), Anthomyiidae (root maggots), Muscidae (house
flies), Calliphoridae (carrion flies), Rhinophoridae (woodlouse flies), Sarcophagidae
(flesh flies) and Tachinidae (tachina flies). The second most common route to parasitoidism in Diptera is through predation, which has been documented seven times
and frequently has been associated with prey items occurring in or on top of the soil.
This route has been inferred for Cecidomyiidae (gall midges), the common ancestor
of Nemestrinidae + Acroceridae (tanglevein flies and spider flies), Bombyliidae
(bee flies) that are also associated with cleptoparasitoidism, Asilidae (robber flies),
Empididae (dance flies), Sciomyzidae (snail-killing flies) and Phacomyiidae (marsh
flies). For dipteran parasitoids, it appears that ants are the most common host group
(Quevillon and Hughes 2018).
A family-level phylogenetic tree of Diptera indicates that ectoparasitoidism originated 10 times, occurring sporadically throughout the phylogeny, whereas endoparasitoidism originated 17 times, largely confined to the Eremoneura (Wiegmann
et al. 2011). This asymmetry in distribution of the two major parasitoid types is
attributable to two major morphological features, the piercing ovipositor of some
Eremoneura (Yeates and Wiegmann 1999), and compensatory behavioral changes
for host seeking in other Eremoneura that lack a penetrative ovipositor (Feener and
Brown 1997). Behavioral features promoting parasitoidization that substitute for a
rigid, puncturing ovipositor include host consumption of parasitoid eggs that hatch
in the gut and invade internal organs (Stireman III et al. 2006), and larvae that
aggressively penetrate the host integument (Feener and Brown 1997; Stireman III
et al. 2006). These features allow Eremoneura to attack and penetrate hosts that
normally would be available only to apocritan Hymenoptera with extensive ovipositor modifications such as lengthening (Eggleton and Belshaw 1992; Feener and
Brown 1997). Most Diptera lack a prolonged, robust ovipositor for penetrating long
distances through indurated tissues as in Hymenoptera, and instead have a flexible,
telescopic ovipositor that is extended by intersegmental membranes, rendering it
inefficient for placing parasitoid eggs deep into host tissue (Feener and Brown
1997). Such ovipositor design restricts many dipteran parasitoid-bearing lineages to
exposed hosts and a preference for ectoparasitoidism over endoparasitoidism, the
latter of which only occasionally occurs across Diptera phylogeny (Eggleton and
Belshaw 1993; Wiegmann et al. 2011). Several derived eremoneuran clades—particularly well developed in Tachinidae (tachina flies), Conopidae, Pipunculidae and
Phoridae (scuttle flies)—have re-evolved stiffened, piercing, albeit undirected, ovipositors with a sclerotized terminus capable of penetrating their hosts (Feener and
Brown 1997; Poinar Jr 2013), allowing for endoparasitoidism. For this reason, there
is the dominance of endoparasitoidism over ectoparasoidism particularly among
Eremoneura (Table 11.1) (Wiegmann et al. 2011). Nevertheless, dipteran parasitoids have never developed capabilities for attacking wood-boring larvae separated
from a bark surface by several centimeters of wood; nor have they been engaged in
penetration of thick, hardened tissues such as galls (Eggleton and Belshaw 1993;
Quicke 1997). However, a substitute for reaching larvae via an ovipositor is hearing
convergence in cricket hosts and their tachina fly parasitoids (Robert et al. 1992).
11 The History of Insect Parasitism and the Mid-Mesozoic Parasitoid Revolution