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5 EarliestEarliest Insects Insects

female (Sturm and Machida, 2001). The ovipositor is used to ARCHAEOGNATHA: THE BRISTLETAILS lay eggs in deep crevices or in holes actually dug by the Bristletails, or Archaeognatha ( Microcoryphia), are the ovipositor. most primitive of living insects, having persisted since at The Archaeognatha consists of only four families and least the mid-Devonian. These cryptic, somewhat cylindrical approximately 500 species: Meinertellidae, Machilidae, Trias- insects occur under loose bark or stones (Figure 5.1). Except somachilidae, and Dasyleptidae (the last two are extinct). The for a rare few, bristletails are nocturnal and typically hide in Meinertellidae occur predominantly in the Southern Hemi- crevices during the day. About 500 species are known world- sphere (Sturm, 1984). The Machilidae, considered by many wide and live in diverse habitats, including elevations as high authors to possess more primitive features than the Mein- as 4,800 meters (15,749 feet) in the Himalayas. The typical ertellidae (e.g., Sturm and Machida, 2001), are mostly found diet of bristletails is composed of algae and lichens, which in the Northern Hemisphere, although a few machilines can they glean using their monocondylic mandibles as picks. be found below the equator in Africa and Asia. While they are not predatory, some species will scavenge Together with silverfish (Zygentoma, which are discussed remains of arthropods and some will even eat their own exu- later), the bristletails comprise the only surviving orders of viae. Major references for the Archaeognatha include primitively wingless insects and were at one time considered accounts by Paclt (1956), Sturm (1984, 1994a,b, 1995a,b, 1997, a single group, Thysanura (e.g., Remington, 1954), as well as 2003a), Kaplin (1985), Mendes (1990, 2002), Sturm and often being united with the Entognatha into a larger group- Bach de Roca (1993), Larink (1997a,b), Bitsch and Nel (1999), ing called the Apterygota, neither of which are monophyletic. and Sturm and Machida (2001). Defining features of the Archaeognatha are the large com- Particularly noteworthy is the mating behavior of pound eyes that meet at the top of the head, and the well- Archaeognatha, which have three principal modes of sperm developed ocelli, both presumably adaptations for nocturnal transfer. Species do not technically copulate, and sperm living. Other features include “jumping,” which is actually a transfer is indirect even though fertilization is internalized. sudden flexion of the abdomen that propels the insect into Males transfer to the female droplets of sperm or sper- the air. Also, the meso- and metapleura consist of a single matophores. Perhaps as a result, the genitalia of archaeog- sclerite with large pleural apodemes. Primitively, the naths are simple and males and females differ relatively little archaeognaths have monocondylic mandibles, the head in the appendicular structures of the genital segments. Cou- skeleton is composed of paired anterior and posterior plates, ples remain in close contact during mating and have distinc- “styli” (exopodites?) are usually on the mid and hind coxae, tive courtship behaviors. In many machilids the males use a and, unlike abdominal styli, these lack musculature. They “carrier-thread” (Sturm, 1952, 1955). The male taps the also have long, seven-segmented maxillary palpi (even female with his maxillary palpi and once she becomes recep- longer than the legs); a terminal filament; eversible vesicles; tive he secretes a thread of silk. The silken line is drawn out, to and abdominal styli (Figure 4.7). Like the Zygentoma, the which the male attaches droplets of sperm. The female is pre- integument of archaeognaths is generally covered with scales vented from moving forward by the male and while the that sometimes form patterns. female is facing away from the thread, the sperm droplets are Even though the putative archaeognaths are among the transferred to her ovipositor and eventually into her gono- oldest fossil insects on record, the overall record of the order pore. In the “firebrat,” Petrobius, the sperm droplets are set is still sparse enough that it has provided little insight into the directly onto the female ovipositor and in Meinertellidae the internal evolution of the order. Among macerated material male creates stalked spermatophores that are retrieved by the taken from the mid-Devonian Gaspé fossil beds of Quebec

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5.1. Representative basal, wingless insects: a bristletail (Archaeognatha) and a silverfish (Zygentoma). These are modern species belonging to groups that evolved at least as early as the Devonian, 400 MYA. Redrawn from Insects of Australia.

were two fragments of a bristletail, a head and thorax, repre- The earliest Mesozoic fossils of the order are Triasso- senting the oldest record of insects in North America machilis uralensis (Triassomachilidae) from the Upper Trias- (Labandeira et al., 1988). The Gaspé fragments, however, pre- sic of Russia (Sharov, 1948). Triassomachilis has at times been serve only primitive features of the Archaeognatha, and no excluded from the Archaeognatha (e.g., Kukalová-Peck, 1991; more conclusive assignment can be made concerning them. Sinitshenkova, 2000c). The fossils are poorly preserved but do Several species from the Carboniferous and Permian are exhibit the dorsal, thoracic hump typical of Archaeognatha as placed in the extinct genus Dasyleptus (Dasyleptidae) (Fig- well as annulated, abdominal styli and a terminal filament in ures 5.2, 5.3). These enigmatic Paleozoic fossils were previ- addition to the long cerci. However, Sharov’s renderings of ously considered to represent an extinct order of mono- the fossils show relatively small compound eyes that do not condylic ectognaths called Monura, closely related to the meet on the vertex, as well as short maxillary palpi, which are Archaeognatha (Sharov, 1957). This position was strongly primitive differences from all other Archaeognatha includ- supported by a reconstruction of Dasyleptus (e.g., Kukalová- ing the much older Dasyleptidae. Paclt (1972) considered Peck, 1987, 1997); however, this intrepretation has been chal- the differences of Triassomachilis and other bristletails to lenged (e.g., Kaplin, 1985; Bitsch and Nel, 1999; Rasnitsyn, be artifacts of preservation misinterpreted by Sharov. The 1999), and, instead, individuals of Dasyleptus appear to be original material should be newly studied to determine typical juvenile silverfish, albeit larger. Rasnitsyn (1999) has the affinities of Triassomachilis and the validity of a family recently reviewed the family Dasyleptidae. Triassomachilidae. CY501-C05[148-154].qxd 2/14/05 4:52 PM Page 150 quark11 27B:CY501:Chapters:Chapter-05:

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5.2. Dasyleptus brongniarti (Dasyleptidae) from the Permian of Russia 5.3. Dasyleptus sharovi from the Early Permian of Elmo, Kansas. MCZ; was formerly placed in an extinct order, Monura, but is today consid- length 11 mm. ered an immature bristletail and a sister group to all other Archaeog- natha. PIN 1197; length 10.5 mm.

All other fossil bristletails occur in Cretaceous or Tertiary (Figure 4.8). The gonangulum represents a basal differentia- ambers. The earliest is a meinertellid in Early Cretaceous tion of the second gonocoxa to form a sclerite with three amber from Lebanon, a species typical of the Machiloides points of articulation – to the ninth abdominal tergum, the group of genera and attesting to the antiquity of this family first gonapophysis, and the second gonocoxa. Other features (Sturm and Machida, 2001). Other Cretaceous amber of dicondylic insects are the reduced maxillary palpi (primi- archaeognaths are known from Burma and New Jersey tively five-segmented, but this is also observed within Entog- (Grimaldi et al., 2000a, 2002). Fossil machilids are also known natha, the Ellipura in particular), and the development of from Baltic amber, while meinertellids are known from tracheal commissures and connectives in the abdomen Dominican amber (e.g., Silvestri, 1912; Sturm and Machida, (Kristensen, 1981). Thus, despite the great overall similarity 2001). Although described as an archaeognath, the Pliocene of bristletails and silverfish, important but subtle features fossil Onychomachilis fischeri (Pierce, 1951) is actually a sil- indicate that silverfish are actually more closely related to verfish, perhaps near the Nicoletiidae (Sturm and Machida, winged insects. 2001).

ZYGENTOMA: THE SILVERFISH DICONDYLIA Silverfish are similar to bristletails in gestalt but are more The traditional taxon Thysanura, or Apterygota, has been rec- flattened; they lack the distinctive hump of the latter group ognized as an unnatural group for decades because silverfish and, therefore, do not jump. Like bristletails, these primi- (Zygentoma) are more closely related to the winged insects tively wingless insects have a long terminal filament (Pterygota) than to the bristletails (e.g., Snodgrass, 1935). In between the cerci and a surface covering of scales (which are his monumental work on the phylogeny and classification of lost in Nicoletiidae and Maindroniidae) (Figures 5.1, 5.4). insects, Hennig (1953, 1969, 1981) proposed the name The biology of the order is superficially similar to that Dicondylia for the group uniting the silverfish with the described for the Archaeognatha, including the occurrence winged insects. Recent molecular studies have also sup- of indirect sperm transfer via a spermatophore; however, ported the Dicondylia as a lineage (e.g., Wheeler et al., 2001). Zygentoma are mostly diurnal and omnivorous with the The hallmark character of this group is the presence of a notable exception of the family Nicoletiidae, which is princi- novel, secondary articulation to the mandible (i.e., the pally subterranean and vegetarian. Though they are not dicondylic mandible) (Figure 5.9). This second articulation capable of jumping, silverfish are very agile and run swiftly, results in the movement of the mandible being roughly con- as anyone who has chased one across a kitchen counter or fined to a single plane of motion rather than the rotating sink knows. In contrast to the Archaeognatha, the com- motion possible in Archaeognatha. It is homologous to the pound eyes are reduced or absent in Zygentoma, and most monocondylic joint in Archaeognatha and Entognatha, families except Lepidotrichidae lack ocelli entirely. Defining since the condyle for the new point of articulation is located features of the silverfish are not immediately apparent, on the head capsule with the acetabulum on the mandible though the enlargement and modification of the distalmost itself. Another significant character defining Dicondylia is palpal segment of the labium and the dorsoventrally flat- the development of the gonangulum in the ovipositor base tened and enlarged coxae may be significant. The enigmatic CY501-C05[148-154].qxd 2/14/05 4:52 PM Page 151 quark11 27B:CY501:Chapters:Chapter-05:

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Lepidotrichidae, and the families Lepismatidae, Nicoletiidae, Ateluridae, and Maindroniidae. The apparently primitive family Lepidotrichidae today is represented by a single mod- ern species living in northern California, Tricholepidion gertschi (Wygodzinsky, 1961) (Figure 5.5), but the family was originally described from a fossil species, Lepidothrix pilifera, in mid-Eocene Baltic amber. This family, however, may not be monophyletic, since Lepidothrix may be more closely related to the remainder of the Zygentoma (Euzygentoma). Tricholepidion possesses distinct ocelli while Lepidothrix and Euzygentoma lack ocelli. Regardless of potential paraphyly of Lepidotrichidae, the family possesses a number of putative primitive features relative to Euzygentoma, including the large abdominal sterna and large number of abdominal styli and eversible vesicles. However, eversible vesicles are only absent in Lepismatidae and Maindroniidae, and this character is shared (primitively?) with Nicoletiidae and Ateluridae. Indeed, Tricholepidion and Nicoletiidae share a unique modification of sensillar structures on the terminal fil- ament (Wygodzinsky, 1961) and the former shares sperm con- jugation with Lepismatidae (Wingstrand, 1973; Kristensen, 5.4. A male and female of the common European silverfish, Thermobia 1997), whereby individual sperm cells pair in the vas deferens domestica (Lepismatidae), as they initiate their courtship. Photo: H. Sturm. of the testes. Evidence for sperm conjugation in Nicoletiidae (Jamieson, 1987) is apparently not conclusive (Dallai et al., 2001). It is possible that Lepidotrichidae is the sister group Lepidotrichidae are at times excluded from the order. Other- to all other Zygentoma, with Nicoletiidae and Ateluridae wise, most differences between Zygentoma and Archaeog- being sister to a clade consisting of Lepismatidae and Main- natha lie in those traits the former shares with winged droniidae. Interestingly, Tricholepidion has five-segmented insects. Major recent references for the Zygentoma include tarsi, like the presumed primitive condition for Pterygota. Mendes (1991, 1994, 2002), Larink (1997a,b), and Sturm Archaeognatha and the remaining silverfish families have (1997, 2003b). two- or three-segmented tarsi, conditions typically inter- The order consists of five Recent families in two groups: preted as derived, independent reductions. Alternatively,

5.5. The relict silverfish, Tricholepidion gertschi (Lepidotrichidae), from California. The only other member of the family is found in Baltic amber, which together may comprise the sister group to the remainder of the order Zygentoma. Photo: H. Sturm. CY501-C05[148-154].qxd 2/14/05 4:52 PM Page 152 quark11 27B:CY501:Chapters:Chapter-05:

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5.7. An immature silverfish (Zygentoma) in Miocene Dominican amber. Morone Collection; length 4 mm.

5.6. A silverfish from Brazil’s Early Cretaceous Santana Formation. Although silverfish undoubtedly are of Devonian age, this relatively although nice compressions of Lower Cretaceous silverfish modern-looking species is among the earliest records of the order have been recovered from the Sanatana Formation of Brazil Zygentoma, leaving a presumed 280 MY gap in their earliest fossil record. AMNH; body length 14 mm. (e.g., Sturm, 1998: Figures 5.6, 5.7). Cuticular fragments from the Devonian of Gilboa, New York, may represent a species of Zygentoma (Shear et al., 1984), but a conclusive assignment but an unlikely scenario, pentamerous tarsi developed remains impossible to make. Similarly, Carbotriplura kukalo- independently in Tricholepidion and Pterygota, or these are vae from the Late Carboniferous of the Czech Republic is sister groups (e.g., Wheeler et al., 2001). likely a silverfish (Kluge, 1996), and although its assignment The Euzygentoma have been defined by the reduction of to Zygentoma is tentative, its placement in a separate subor- the abdominal sterna (although this also occurs in Archaeog- der of wingless insects is unjustified. The Pliocene fossil Ony- natha), the reduced number of abdominal styli, and the chomachilis fischeri was described as a bristletail (Pierce, absence of ocelli. Reduction in the number of tarsomeres 1951) but is actually a silverfish (Sturm and Machida, 2001). may also represent a defining feature of this lineage. The Maindroniidae is a rare family of three species restricted from Asia Minor and Chile. Little is known or understood of these RHYNIOGNATHA presumed relics, but they may be derivatives of the Lepis- matidae (e.g., Remington, 1954). The Lepismatidae is the Rhyniella, the collembolan in Early Devonian Rhynie chert, largest family of the order, with over 200 species worldwide has long been heralded as the oldest hexapod, while frag- and as such are the group most frequently encountered. mentary remains from the same chert had been mostly for- The families Nicoletiidae and Ateluridae are close relatives, gotten. In the original paper announcing the discovery of both lacking eyes and at times having been included in a sin- Rhyniella, Hirst and Maulik (1926) also reported a pair of gle family (e.g., Remington, 1954; Paclt, 1963, 1967). The mandibles preserved with largely unidentifiable tissues sur- Nicoletiidae are, like the lepismatids, cosmopolitan in distri- rounding them (Figure 5.8). Later, Tillyard (1928b) formally bution. Interestingly, some nicoletiids can reproduce described the mandibular elements and named them, parthenogenetically. Ateluridae are inquilines that live in Rhyniognatha hirsti. Tillyard was the first to note that they subterranean ant and termite nests, though a few lepismatids were insect-like, but he did not place them formally into any are also inquilines. group. Indeed, subsequent authors relied on Tillyard’s illus- Despite the apparent antiquity of Zygentoma as the sister tration and followed his intrepretation that the mandibles group to all other dicondylic insects, there is a huge gap in were “suggestive” of an insect (e.g., Hennig, 1981). Most their early fossil record. We would expect to find fossil Zygen- authors, however, considered Rhyniognatha as too fragmen- toma as early as the Devonian, but their fossil record is tary to make any determination, and Carpenter (1992) almost entirely restricted to Cretaceous and Tertiary resins even excluded it from his monumental treatise on insect (e.g., Mendes, 1997, 1998; Sturm and Mendes, 1998), paleontology. CY501-C05[148-154].qxd 2/14/05 4:52 PM Page 153 quark11 27B:CY501:Chapters:Chapter-05:

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5.8. The oldest insect, Rhyniognatha hirsti, from the Early Devonian chert near Rhynie, Scotland. Only portions of the head are preserved, but the dicondylic mandibles indicate it was an insect; their triangular shapes indi- cate it may even have been a winged insect. NHML In. 38234.

In a recent study of the unique holotype of Rhyniognatha group among the pterygote insects, the Metapterygota, (Engel and Grimaldi, 2004a), the presence of an anterior implying that Rhyniognatha possessed wings. This would acetabulum and posterior condyle on the mandibles was con- place the origin of wings at least 80 million years earlier than firmed, conclusively demonstrating that the mandibles are previous fossil evidence allowed, and interestingly agrees dicondylic (Figures 5.8, 5.9). Furthermore, the mandibles are with a recent molecular study that estimated insects origi- short and triangular, a morphology characteristic of a subset nated in the Early Silurian and neopterous insects in the CY501-C05[148-154].qxd 2/14/05 4:53 PM Page 154 quark11 27B:CY501:Chapters:Chapter-05:

154 EVOLUTION OF THE INSECTS COLLEMBOLA PROTURA DIPLURA ARCHAEOGNATHA ZYGENTOMA EPHEMEROPTERA METAPTERYGOTA DEVONIAN

5.9. Phylogeny of basal insect lineages indicating the position of Rhyniognatha, the oldest insect, as based on the structure of mandibles. Fossils (numbers): 1. Rhyniella praecursor; 2,3. undescribed; 4. Rhyniognatha hirsti. Characters (letters): A. insectan (see text), B. dicondylic mandibles, C. wings, D. entognathous mouthparts.

mid-Devonian (Gaunt and Miles, 2002) (see also the Origin of derived than bristletails and silverfish, and probably more Wings in Chapter 6). A Devonian origin of wings could only than Ephemeroptera. Regardless, Rhyniognatha’s occur- be conclusively proven with fossilized wings from that rence in the Early Devonian indicates that insects likely period. originated in the latest Silurian and were among the earli- It is impossible to say to what order Rhyniognatha might est of terrestrial faunas (Engel and Grimaldi, 2004a). have belonged, or if it belonged to an unknown, extinct lin- Rhyniognatha also reflects the serious need for intensive eage of primitive insects. All than can be said is that exploration of insects from the Devonian and Early Car- Rhyniognatha is the oldest insect, and that it was more boniferous.