Insect evolution

  The relationships of insects to other animal groups remain unclear. Although more traditionally grouped with millipedes and centipedes, evidence has emerged favouring closer evolutionary ties with the crustaceans. In the Pancrustacea theory, insects, together with among others Malacostraca, make up a monophyletic group (sharing a common ancestor).

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Early evidence

The oldest definitive insect fossil is the Devonian Rhyniognatha hirsti, estimated at 396-407 million years old.^[1] This species already possessed dicondylic mandibles, a feature associated with winged insects, suggesting that wings may already have evolved at this time. Thus, the first insects probably appeared earlier, in the Silurian period.^[1]

The subclass Apterygota (wingless insects) is now considered artificial as the silverfish (order Thysanura) are more closely related to Pterygota (winged insects) than to bristletails (order Archaeognatha). For instance, just like flying insects, Thysanura have so-called dicondylic mandibles, while Archaeognatha have monocondylic mandibles. The reason for their resemblance is not due to a particularly close relationship, but rather because they both have kept a primitive and original anatomy in a much higher degree than the winged insects. The most primitive order of flying insects, the mayflies (Ephemeroptera), are also those who are most morphologically and physiologically similar to these wingless insects. Some mayfly nymphs resemble aquatic thysanurans.

Modern Archaeognatha and Thysanura still have rudimentary appendages on their abdomen called styli, while more primitive and extinct insects known as Monura had much more developed abdominal appendages, as seen here. The abdominal and thoracic segments in the earliest terrestrial ancestor of the insects would have been more similar to each others than they are today, and the head had well developed compound eyes and long antennae. Their body size is not known yet. As the most primitive group today, Archaeognatha, is most abundant near the coasts, it could mean that this was the kind of habitat where the insect ancestors became terrestrial. But this specialization to coastal niches could also have a secondary origin, just as could their jumping locomotion, as it is the crawling Thysanura who are considered to be most original (plesiomorphic). By looking at how primitive cheliceratan book gills (still seen in horseshoe crabs) evolved into book lungs in primitive spiders and finally into tracheae in more advanced spiders (most of them still have a pair of book lungs intact as well), it is possible the trachea of insects was formed in a similar way, modifying gills at the base of their appendages.

So far there is nothing that suggests the insects were a particularly successful group of animals before they got their wings.

Odonata

The Odonata (dragonflies) are also a good candidate as the oldest living member of the Pterygota. Mayflies are morphologically and physiologically more primitive, but the derived and advanced characteristics of dragonflies could have evolved independently in their own direction for a long time. It seems that orders with aquatic nymphs or larvae become evolutionarily conservative once they had adapted to water. If mayflies made it to the water first, this could partly explain why they are more primitive than dragonflies, even if dragonflies have an older origin.

Similarly, stoneflies are the most primitive of the Neoptera, but they were not necessarily the first order to branch off. This also makes it less likely that an aquatic ancestor would have the evolutionary potential to give rise to all the different forms and species of insects that we know today.

Dragonfly nymphs have a unique labial "mask" used for catching prey, and the imago has a unique way of copulating, using a secondary male sex organ on the second abdominal segment. It looks like abdominal appendages modified for sperm transfer and direct insemination have occurred at least twice in insect evolution, once in Odonata and once in the other flying insects. If these two different methods are the original ways of copulating for each group, it is a strong indication that it is the dragonflies who are the oldest, not the mayflies. There is still not agreement about this. Another scenario is that abdominal appendages adapted for direct insemination has evolved three times in insects; once Odonata, once in mayflies and once in the Neoptera, both mayflies and Neoptera choosing the same solution. If so, it is still possible that mayflies are the oldest order among the flying insects. The power of flight is assumed to have evolved only once, suggesting sperm transfer in the earliest flying insects still was done indirectly.

One possible scenario on how direct insemination evolved in insects is seen in scorpions. The male deposits a spermatophore on the ground, locks its claws with the female's claws and then guides her over his packet of sperm, making sure it comes in contact with her genital opening.

When the early (male) insects laid their spermatophores on the ground, it seems likely that some of them used the clasping organs at the end of their body to drag the female over the package. The ancestors of Odonata evolved the habit of grabbing the female behind her head, as they still do today. This action, rather than not grasping the female at all, would have increased the male's chances of spreading its genes. The chances would be further increased if they first attached their spermatophore safely on their own abdomen before they placed their abdominal claspers behind the female's head; the male would then not let the female go before her abdomen had made direct contact with his sperm storage, allowing the transfer of all sperm.

This also meant increased freedom in searching for a female mate because the males could now transport the packet of sperm elsewhere if the first female slipped away. This ability would eliminate the need to either wait for another female at the site of the deposited sperm packet or to produce a new packet, wasting energy. Other advantages include the possibility of mating in other, safer places than flat ground, such as in trees or bushes.

If the ancestors of the other flying insects evolved the same habit of clasping the female and drag her over their spermathophore, but posterior instead of anterior like the Odonata does, their genitals would come very close to each others. And from there on, it would be a very short step to modify the vestigial appendages near the male genital opening to transfer the sperm directly into the female. The same appendages the male Odonata use to transfer their sperm to their secondary sexual organs at the front of their abdomen.

All insects with an aquatic nymphal or larval stage seem to have adapted to water secondarily from terrestrial ancestors. Of the most primitive insects with no wings at all, Archaeognatha and Thysanura, all members live their entire life cycle in terrestrial environments. As mentioned previously, Archaeognatha were the first to split off from the branch that led to the winged insects (Pterygota), and then the Thysanura branched off. This indicates that these three groups (Archaeognatha, Thysanura and Pterygota) have a common terrestrial ancestor, which probably resembled a primitive model of Apterygota, was an opportunistic generalist and laid spermatophores on the ground instead of copulating, like Thysanura still do today. If it had feeding habits similar to the majority of apterygotes of today, it lived mostly as a decomposer.

One should expect that a gill breathing arthropod would modify its gills to breathe air if it were adapting to terrestrial environments, and not evolve new respiration organs from bottom up next to the original and still functioning ones.

Then comes the fact that insect (larva and nymph) gills are actually a part of a modified, closed trachea system specially adapted for water, called tracheal gills. The arthropod trachea can only arise in an atmosphere and as a consequence of the adaptations of living on land. This too indicates that insects are descended from a terrestrial ancestor.

And finally when looking at the three most primitive insects with aquatic nymphs (called naiads: Ephemeroptera, Odonata and Plecoptera), each order has its own kind of tracheal gills that are so different from one another that they must have separate origins. This would be expected if they evolved from land-dwelling species.

This means that one of the most interesting parts of insect evolution is what happened between the Thysanura-Pterygota split and the first flight.

Origin of insect flight

The origin of insect flight remains obscure, since the earliest winged insects currently known appear to have been capable fliers. Some extinct insects (e.g. the Palaeodictyoptera) had an additional pair of winglets attached to the first segment of the thorax, for a total of three pairs.

The wings themselves are thought by many to be highly modified (tracheal) gills. And there is no doubt that the tracheal gills of the mayfly nymph in many species look like wings. By comparing a well developed pair of gill blades in the naiads and a reduced pair of hind wings on the adults, it is not hard to imagine that the mayfly gills (tergaliae) and insect wings have a common origin, and newer research also supports this. The tergaliae are not found in any other order of insects, and they have evolved into different directions with time. In some nymphs/naiads the most anterior pair has become sclerotized and works as a gill cover for the rest of the gills. Others can form a large sucker, be used for swimming or modified into other shapes. But it doesn't have to mean that these structures were originally gills. It could also mean that the tergaliae evolved from the same structures which gave rise to the wings, and that flying insects evolved from a wingless terrestrial species with pairs of plates on its body segments: three on the thorax and nine on the abdomen (mayfly nymphs with nine pairs of tergaliae on the abdomen exist, but so far no living or extinct insects with plates on the last two segments have been found). If these were primary gills, it would be a mystery why they should have waited so long to be modified when we see the different modifications in modern mayfly nymphs.

Theories

When the first forests arose on earth, new niches for terrestrial animals were created. Spore-feeders and others who depended on plants and/or the animals living around them would have to adapt too to make use of them. In a world with no flying animals, it would probably just be a matter of time before some arthropods who were living in the trees evolved paired structures with muscle attachments from their exoskeleton and used them for gliding, one pair on each segment. Further evolution in this direction would give bigger gliding structures on their thorax and gradually smaller ones on their abdomen. Their bodies would have become stiffer while thysanurans, which didn't evolve flight, kept their flexible abdomen.

Mayfly nymphs must have adapted to water while they still had the "gliders" on their abdomen intact. So far there is no concrete evidence to support this theory either, but it is one that offers an explanation for the problems of why presumably aquatic animals evolved in the direction they did.

Leaping and arboreal insects seems like a good explanation for this evolutionary process for several reasons. Because early winged insects were lacking the sophisticated wing folding mechanism of neopterous insects, they must have lived in the open and not been able to hide or search for food under leaves, in cracks, under rocks and other such confined spaced. In these old forests there weren't many open places where insects with huge structures on their back could have lived without experiencing huge disadvantages. If insects got their wings on land and not in water, which clearly seems to be the case, the tree canopies would be the most obvious place where such gliding structures could have emerged, in a time when the air was a new territory. The question is if the plates used for gliding evolved from "scratch" or by modifying already existing anatomical details. The thorax in Thysanura and Archaeognatha are known to have some structures connected to their trachea which share similarities to the wings of primitive insects. This suggests the origin of both the wings and the spiracles are related.

Gliding requires universal body modifications, as seen in present-day vertebrates such as some rodents and marsupials, which have grown wide, flat expansions of skin for this purpose. The flying dragon of Indonesia has modified its ribs into gliders, and even some snakes can glide through the air by spreading their ribs. The main difference is that while vertebrates have an inner skeleton, primitive insects had a flexible and adaptive exoskeleton.

It is clear that there would have been some animals living in the trees, as animals are always taking advantage of all available niches, both for feeding and protection. At the time, the reproductive organs were by far the most nutritious part of the plant, and these early plants show signs of arthropod consumption and adaptations to protect themselves, for example by placing their reproductive organs as high up as possible. But there will always be some species who will be able to cope with that by following the their food source up the trees.

Knowing that insects were terrestrial at that time and that some arthropods (like primitive insects) were living in the tree crowns, it seems less likely that they would have developed their wings down on the ground or in the water.

In a three dimensional environment such as trees, the ability to glide would increase the insects' chances to survive a fall, as well as saving energy. This trait has repeated itself in modern wingless species such as the gliding ants who are living an arboreal life. When the gliding ability first had originated, gliding and leaping behavior would be a logical next step, which would eventually be refelcted in their anatomical design.

The need to navigate through vegetation and to land safely would mean good muscle control over the proto-wings, and further improvements would eventually lead to true (but primitive) wings.

While the thorax got the wings, a long abdomen could have served as a stabilizer in flight.

It is also worth remembering that some of the earliest flying insects were large predators. This isn't surprising since there weren't any yet any other predators hunting in the air: it was therefore a totally new ecological niche. Some of the prey were without a doubt other insects, as insects with proto-wings would have radiated into other species even before the wings were fully evolved. From this point onwards, the arms race could continue: the same predator/prey co-evolution which has existed as long as there have been predators and prey on earth; both the hunters and the hunted were in need of improving and extending their flight skills even further to keep up with the other.

Insects that had evolved their proto-wings in a world without flying predators could afford to be exposed openly without risk, but this changed when carnivorous flying insects evolved. It is unknown when they first evolved, but once these predators had emerged they put a strong selection pressure on their victims and themselves. Those of the prey who came up with a good solution about how to fold their wings over their backs in a way that made it possible for them to live in narrow spaces would not only be able to hide from flying predators (and terrestrial predators if they were on the ground) but also to exploit a wide variety of niches that were closed to those who couldn't fold their wings in this way. And today the neopterous insects (those that can fold their wings back over the abdomen) are by far the most dominant group of insects.

Another theory, the so-called water-skimming theory, suggesting skimming on the water surface as the origin of insect flight seems elegant, but there is, so far, nothing to support it.

Life cycle

Mayflies

Another primitive trait of the mayflies are the subimago; no other insects have this winged yet sexually immature stage. A few specialized species have females with no subimago, but retain the subimago stage for males.

The reasons the subimago still exists in this order could be that there hasn't been enough selection pressure to get rid of it; it also seems specially adapted to do the transition from water to air.

The male geniatalia are not fully functional at this point. One reason for this could be that the modification of the abdominal appendages into male copulation organs emerged later than the evolution of flight. This is indicated by the fact that dragonflies have a different copulation organ than other insects.

As we know, in mayflies the nymphs and the adults are specialized for two different ways of living; in the water and in the air. The only stage (instar) between these two is the subimago. In more primitive fossil forms, the preadult individuals had not just one instar but numerous ones (while the modern subimago do not eat, older and more primitive species with a subimagos were probably feeding in this phase of life too as the lines between the instars were much more diffuse and gradual than today). Adult form was reached several moults before maturity. They probably didn't have more instars after becoming fully mature. This way of maturing is how Apterygota do it, which moult even when mature, but not winged insects.

Modern mayflies have eliminated all the instars between imago and nymph, except the single instar called subimago, which is still not (at least not in the males) fully sexually mature. The other flying insects with incomplete metamorphosis (Exopterygota) have gone a little further and completed the trend; here all the immature structures of the animal from the last nymphal stage are completed at once in a single final moult. The more advanced insects with larvae and complete metamorphosis (Endopterygota) have gone even further. An interesting theory here is that the pupal stage is actually a strongly modified and extended stage of subimago, but so far it is nothing more than a theory. Interestingly enough there are some insects within the Exopterygota, thrips and whiteflies (Aleyrodidae), who have evolved pupae-like stages too.

Distant ancestors

The distant ancestor of flying insects, a species with primitive proto-wings, had a more or less ametabolous life cycle and instars of basically the same type as thysanurans with no defined nymphal, subimago or adult stages as the individual became older. Individuals developed gradually as they were growing and moulting, but there were probably no big changes in between instars.

Modern mayfly nymphs do not acquire gills until after their first moult. Before this stage they are so small that there is no need for gills to extract oxygen from the water. This could be a trait from the common ancestor all flyers evolved from. An early terrestrial insect would have no need for paired outgrowths from the body before it started to live in the trees (or in the water, for that matter), so it would not have any.

This would also affect the way their offspring looked like in the early instars, resembling earlier ametabolous generations even after they had started to adapt to a new way of living, in a habitat where they actually could have some good use for flaps along their body. Since they matured in the same way as thysanurans with plenty of moultings as they were growing and very little difference between the adults and much younger individuals (unlike modern insects, who are hemimetabolous or holometabolous), there probably wasn't much room for adapting into different niches depending on age and stage. Also, it would have been difficult for an animal already adapted to a niche to make a switch to a new niche later in life based on age or size differences alone when these differences were not significant.

So they had to specialize and focus their whole existence on improving a single lifestyle in a particular niche. The older the species and the single individuals became, the more would they differ from their original form as they adapted to their new lifestyle better than the generations before. The final body design was no longer achieved while still inside the egg, but continued to develop for most of the life, causing a bigger difference between the youngest and oldest individuals. Assuming that mature individuals most likely mastered their new element better than did the nymphs who had the same lifestyle, it would appear to be an advantage if the immatures reached adult shape and form as soon as possible. This may explain why they evolved fewer but more intense instars and a stronger focus on the adult body, and the differences between the adults and the first instars were greater, instead of just gradually growing bigger as earlier generations had done. This evolutionary trend explains how they went from ametabolous to hemimetabolous insects.

Reaching maturity and a fully grown body became only a part of the development process, gradually also a new anatomy and new abilities only possible in the later stages of life, were included. The anatomy they were born and grew up with had limitations the adults who had learned to fly didn't have. If they couldn't live their early life the way adults did, immature individuals had to adapt to the best way of living and surviving despite their limitations till the moment came when they could leave them behind. This would be a starting point in the evolution where imago and nymphs started to live in different niches, some more clearly defined than others. Also, a final anatomy, size and maturity reached at once with a single final nymphal stage meant less waste of time and energy, and also made a more complex adult body structure. These strategies obviously became very successful with time.

Late Carboniferous and Early Permian insect orders include both several current very long-lived groups (mayflies, (Ephemeroptera), dragonflies (Odonata), cockroaches (Blattodea), and Orthoptera (grasshoppers and their relatives)) and a number of Paleozoic forms. During this era, some giant dragonfly-like forms – e.g. Meganeura and Meganeuropsis (Order Protodonata) and Mazothairos (Order Palaeodictyoptera) – reached wingspans of 55 to 70 cm (22 to 28 in), making them far larger than any living insect. Also their nymphs must have had a very impressive size. This gigantism may have been due to higher atmospheric oxygen levels (up to 80% above modern levels during the Carboniferous) that allowed increased respiratory efficiency relative to today. The lack of flying vertebrates could have been another factor.

Most extant orders of insects developed during the Permian era that began around 270 million years ago. Many of the early groups became extinct during the Permian-Triassic extinction event, the largest mass extinction in the history of the Earth, around 252 million years ago.

The remarkably successful Hymenopterans appeared in the Cretaceous but achieved their diversity more recently, in the Cenozoic. A number of highly successful insect groups — especially the Hymenoptera and Lepidoptera (butterflies), as well as many types of Diptera (flies) and Coleoptera (beetles) — evolved in conjunction with flowering plants, a powerful illustration of co-evolution.

Many modern insect genera developed during the Cenozoic; insects from this period on are often found preserved in amber, often in perfect condition. Such specimens are easily compared with modern species. The study of fossilized insects is called paleoentomology.

See also

• Butterfly evolution
• Spider evolution

References

• Grimaldi, David and Michael S. Engel (2005-05-16). Evolution of the Insects. Cambridge University Press. ISBN 0-521-82149-5.  — an up to date review of the evolutionary history of the insects
• Rasnitsyn, A.P. and Quicke, D.L.J. (2002). History of Insects. Kluwer Academic Publishers. ISBN 1-4020-0026-X.  — detail coverage of various aspects of the evolutionary history of the insects