The Primitive Characters of Extant Mayflies (Ephemeroptera)
Abstract
The primitive characters remain in extant mayflies are discussed; the important opinions and explanations of them are referred and compared; the research importance and necessary of mayflies to the understanding of origin and evolution of Pterygota and Insecta is emphasized.
Mayflies (Insecta: Ephemeroptera) are living fossils of Insecta (You et Gui 1979, 1995; Gui et You 1982). Because they have some significant primitive characters, the entomologists have paid great attention to studying them for long time. In 1661, Dutch entomologist, Jan Swammerdam began to study the mayflies, his famous picture of anatomy of Palingenia longicauda Oliver was published in 1738. Those primitive characters of them contribute greatly to explanation of the origin and evolution of insects, insect wings and intra-relationship of Insecta.
Unfortunately, partly because the Chinese mayflies are poor known, the primitive characters of extant mayflies are not reported as a whole deeply in China. Only some of them, for example, the long segmented caudal filaments, the 7 pairs abdominal gills, wing veins and wing position were often cited or proposed in various papers. The following of this paper deal with this theme.
Prometabola
The life cycle of mayflies includes four stages: egg, nymph, subimago and imago. This unique metamorpha is called prometabola. That means the mayflies have two separate adult instars.
All male mayflies and most females moult from subimago to imago. Females of a few specialized species have lost the imago (Edmunds et McCafferty 1988). There are some differences between the subimago and imago (please see paper of Edmunds et McCafferty 1988 for details). Among them, two are important: the one is that the male subimago lacks the fully developed external genitalia. The fully formed male genitalia, including the female-clasping forceps, in subimago of any species are never found. The other is the subimaginal wings are with falciform microtrichia and its surface with fine cilia. The body of subimago with surface setae too. The wings and body of male imago are without any of them. The hairy surface of the body, legs and wings of the subimago would allow the mayflies overcome the hazards of emergence: the presence of the setae, cilia and microtrichia suggest that subimago is much fore effective hydrofuge from the adult. The study shows that the male genitalia grow in a paurometobolous fashion rather than being prepackaged like legs and wings. We must assume that two moults from the larval stage are required for males to attain reproductive maturity and function. Thus the subimago has at least some necessary role in transformation (Edmunds et McCafferty 1988).
Scharfer(1975) suggested that the functional genitalia and wings of mayflies do not be mature simultaneously is a relic of ancient double moult: the wings occur first , after the second moult the genitalia are functional. While in other insects, they occur in only one moult. The selection pressure did not affect the ephemerous beings, the mayflies, greatly.
Cheng (1955) and Tan (1980) proposed that the subimago of mayflies is equivalent to the pupa of Holometabola. So they assumed that the Heterometabola and Holometabola all originated from the Prometabola.
But Kukalová-Peck (1978, 1994) believed that all metamorphosis, including Prometabola, originate from the Ametabola. She has presented convincing fossil data in support of a primitive existence of subimago. In early fossil Ephemeroptera or Ephemeroptera precussors, the developing wings of immature forms were freely articulated with the thorax, and wing development proceeded gradually through numerous moults. The preadult instars with articulated wings as subimagos have several instars. The modern mayflies have only one instar is the result of evolution.
Number of moults
Mayflies have a large number of postembryonic moults (10-50), most species are in the range 15-25 (Brittain 1982).
Kukalová-Peck (1978, 1994) and Hubbard et Kukalová-Peck (1980) suggested that the Palaeozoic Palaeoptera (including Ephemeroptera) with permanently outstretched wings had the following peculiar development. The wings in young nymphs were arched backwards, the arch (nymphal wing bend) straightened a little in each subsequent instar, until the wings were fully outstretched. In the absence of a metamorphic moult, this required many nymphal and subimaginal instars. Later under the selection pressure, most insects tend to reduce the times of moults and the metamorphysis established. But the mayflies remain this primitive habitat.
Chen (1955), Tian(1980) and some others assumed that the Pterygota originated from the Zygentoma. Zygentoma is ametamorphic group and moult many time in life cycle. The extant Ephemeroptera, which is the most primitive group of Pterygota, remain a large number of nymphal moults.
Wing venation and wing corrugation
The main longitudinal veins of fore wing of extant mayflies are including C, Sc, R, MA (MA1 and MA2), MP (MP1 and MP2), CuA, CuP, A (the J is very weak or short and can not be distinguished). The wings of most mayflies with a lots of cross-veins. Besides those, the wing is with a Humeral cross-vein, some intercalaries and marginal intercalaries. More or less corrugation remained on the wing.
Kukalová-Peck (1994) suggested that the primitive insect wing with eight pairs of longitudinal veins. They are PC (PCA+, PCP-), C(CA+, CP-), Sc(ScA+,ScP-), R(RA+, RP-), M(MA+, MP-), Cu(CuA+,CuP-), A(AA+, AP-), J(JA+, JP-). The fore vein in each pair is convex, the hind vein is concave. So the wing with deep corrugation. Because of evolution and need of efficient flight, the PC, C and ScA fused together forming the strong costal margin. The Humeral cross-vein of mayflies originated from the ScA+. It links the C,Sc and R together. From the above, we can see that the wing venation of mayflies keeps the main pattern of venation and corrugation of primitive insect wing.
Wing articulation and wing position
Without the flexing wing sclerites and muscles, Mayflies hold their wings vertically upwards when they are at rest, can not flex their wings backwards on the abdomen like the Neoptera.
This character is often cited as primitive one by many Entomologists. But according to Kukalová-Peck, this is not true.
TKukalová-peck (1994) reported that the wing articulations of modern Pterygota were homologised. The most primitive Pterygota wing articulation is believed to be a densely crowed band of articulated sclerites surrounding the wing like a horseshoe. The individual dorsal sclerites are similar in size and form 8 rows, each of 4 sclerites: Proxalaria, Axaliria, Fulcularia and Basivenalia. These rows cover blood channels and distal sclerite of each row is also a blood sinus for one of the 8 veinal pairs.
The articular plate of modern Ephemeroptera consists of the Basivenalia and Fulcalria of Sc, R and M, with those of Cu, A and J stiffly hinged posteriorly, two columns of free sclerites (Proxalaria and Axalaria) are articulated mainly in rows aligned with veins in Palaeozoic mayflies. But this pattern is disrupted by desclerotistion in recent forms, which may still retain Fulcularia musculature. So we can see that, at the base of wing, there are a small costal plate (align the C) and a bigger articulation plate(align the Sc,R,M,Cu,A). The longitudinal veins of fore wing (except C) seemed like originating from the same point of wing base.
So although the mayflies and some ancestral insects hold their wings vertically upwards when they are at rest, this is not the ancient. It also a derived character from primitive groundplan.
Appendages
Besides the antennae, legs and wings, the mayflies have some other appendage-like structures on their thorax and abdomen. For example, the 7 pairs of gills, one pair of forceps and one pair of long multi-segmented cerci. Where did they come from? Are they homologous?
According to groundplan of Hexapoda leg established by Kukalová-Peck (1994), an ancestral arthropodan leg which contained in its groundplan no fewer than 11 segments and an unknown number of outer and inner annulated lobes. So the two pairs wings and seven pairs of gills of mayflies nymphs originated from the epicoxa exite. The legs, forceps and cerci derived from leglets are articulated to body by means of coxa. The penes are homologous with 10th trochanter endites. The gill tufts (for instance, of the species in genus Isonychia, Isonychiidae) are homologous with coxal endites. The terminal filament of mayfly is the expansion of the last abdominal segment.
The abdominal gills of nymphs are homologous with thoraxal wings (Wigglesworth 1973; Kukalová-Peck 1978, 1994). Because:1. The shape of gill-plates very like the wings, they are all with veins (especially in Palaeozonic mayflies), leading margin is often strengthened; 2. The gill-plates are segmentally arranges, articulated and moved by subcoxo-coxal muscles; 3. nymphs never develop gill-plates on the thorax or head; 4. The location of them are between the subcoxa and the tergum, always above the spiracles; 5. Some extant mayfly adults remain "gills" in their abdomen.
The mayflies maybe originated from the Zygentoma (Chen 1955; Wigglesworth 1973; Tian 1980). They are all with long caudal filaments. In other insect orders, the cerci are very short. If we consider that the unique mating behavior (Brinck 1957), the empty guts, and light body of mayfly adults, we may believe that the long caudal filaments may be important roles in keeping the balance.
The tracheae in wings
Whitten(1962) reported that the all veins of each wing of mayflies are supplied by one thachea from the one spiracle. The fore wing's trachea from the anterior spiracle,and the hind wing from the posterior one. In other words, the tracheation in Ephemeroptera is restricted in each somite (prosegment) to that of its own spriacle. This condition is most likely to be close to the archetype stage, and thus to be more primitive than that of the Pterygota. In other insects, each fore and hindwing isserved by two tracheae: the anterior trachea supplies the oxygen to the Costa-Media vention, and the posterior trachea supplies oxygen to Cubito-Anal venation.
Blood flow in wing vein
In mayflies, the general loop-like blood flow, which is similar to that in all other modern orders, often alternates with an intermittent refluxing of blood into and out of the wing. This exceptional phenomenon has been attributed to broad basal sinus, a primitive character in Palaeozonic insects.Reproductive system
Mayflies have panoistic ovarioles, the reproductive system of them without accessory glands, and the gonoducts are paired in both sexes, each duct opening to the exterior separately; ovipositor is always absent.
Mouthparts
Three-lobed membranal hypopharynx; the galea and lacinia of mandible fused together. This character is primitive according to Wille(1960, mentioned by Hennig 1981).
The Malpighian tubes number up to 140 (Landa 1969; Britten 1982).
Conclusion
Because of above mentioned, we can conclude that the extant mayflies remain many primitive characters. They are relics of primitive Pterygota. Those make them the good materials for explaining the origin and evolution of Insecta.
REFERENCES
Brinck P. 1957. Reproductive system and mating in Ephemeroptera. Opuscula Entomol., 22:1-37
Brittain J E. 1982. Biology of Mayflies. Ann.Rev.Entomol.,27:119-147
Chen Shi-xiang. 1955. The origin and evolution of the Class Insecta. Acta Entomologica Sicica, 5(1):1-43
Edmunds G F Jr, W P McCafferty. 1988. The mayfly subimago. Ann. Rev. Entomol, 33:509-529
Gui Hong,You Da-shou. 1982. Mayflies. Insects knowledge, 6:33-37
Hennig W. 1981. Insect Phylogeny. Translated and edited by A.C.Pont. John Wiley & Sons Press
Hubbard M, J Kukalová-Peck. 1980. Permian mayfly nymphs: new taxa and systematic characters. Pages19-31. In J.F.Flannagan & K.E. Marshall,eds, Adances in Ephemeroptera Biology, Plenum Press, New York
Kukalová-Peck J.1978. Origin and evolution of insect wings and their relation to Metamorphosis, as documented by the fossil record. J. Morphol., 156:53-125.
Kukalová-Peck J.1994. Fossil History and the Evolution of Hexapod Structures. In I.D.Naumann(ed.):Systematic and Applied Entomology.P.133-171
Landa V. 1969. Comparative anatomy of mayfly larvae(Ephemeroptera). Acta entomol. Bohemslav., 66:289-316
Schaefer C W. 1975.The mayfly submago:a possible explanation. Ann. ent. Soc. Am., 68,183
Tian Juan-ji. 1980. A review of the geological history of Insects. Acta Zootaxonomica Sinica, 5(1):1-13
Whitten J M. 1962. Homomogy and development of insect wing tracheae. Ann.Entomol. Soc. Amer., 55:288-295
Wigglesworth V B. 1973. Evolution of insect wings and flight. Nature, 246(5429):127-129
You Da-shou,Gui Hong. 1979. Introduction of the mayfly and its research situation. J. Nanjing Normal College(nature science), 1: 57-63
You Da-shou,Gui Hong. 1995. Economic insect fauna of China. Fasc.48 Ephemeroptera. Science press, Beijing, Pp.152