Evolutionary adaptations of feeding in insects

Over millions of years, insects have got adapted to countless ecological changes. On previous articles, we talked about flying adaptations in insects and how flying made them more diverse. In this new article, we explain you the origin and evolutionary changes of insects’ mouthparts and therefore of feeding diversification throughout their evolutionary history.

Introduction: Entognatha vs Ectognatha

Before talking about feeding evolution of insects, we must state the differences between the terms “insect” and “hexapod”. Insects constitute the major and most diverse class of the subphylum Hexapoda. This class includes the best known families of insects: lepidopteran, hymenopteran, coleopteran, dipteran, etc. However, this subphylum also includes three orders of wingless arthropods which together constitute the class Entognatha: Collembola (springtails), Protura and Diplura.

So, the subphylum Hexapoda includes two classes: Insecta and Entognatha. Which is the main difference between them? Essentially, the position of their mouthparts: on one hand, Entognatha (ento- ‎(“inside”) +‎ Ancient Greek gnáthos (“jaw”)) have their mouthparts protected inside the head and they only project them during feeding; on the other hand, Ectognatha or Insecta (ecto- ‎(“outside”)) always have external mouthparts.

Mouthparts of a beetle (Ectognatha, left) and anterior view of a springtail, with mouthparts retracted within the head (Entognatha, right). Source: beetle by Fyn Kynd Photography, CC; springtail by Gilles San Martin, CC.

Mouthparts of insects or Ectognatha

Both mouthparts diversification and feeding diversification are the result of a long evolutionary process. So, it’s expected that there exist ancestral and derived feeding structures.

The most ancestral mouthparts and those which has also suffered less adaptive modification are the mandibulate or chewing ones. These type of mouthparts are linked to solid food-based feeding and they can be currently observed in a lot of groups: crickets and grasshoppers; dragonflies and damselflies; beetles; cockroaches and mantis; mecopterans, neuropterans… and also in larval stages of some insects that develop a different type of mouthparts when reaching adulthood (e.g. butterfly larvae).

Mandibulate mouthparts are often used as a model to explain the evolution of mouthparts in insects due to their ancestral origin. The most used chewing model is the one observed on orthopterans (such as locusts or grasshoppers).

Mandibulate or chewing model of an orthopteran. Source: John R. Meyer, North Carolina State University. Link.

Based on this model, insect’s mouthparts are made of 5 main structures: labrum, mandibles, maxillae, hypopharynx and labium. Mandibles, maxillae and labium are considered true or appendicular appendages because they develop from metameres (also known as somites; segments in which their body is divided) during the embryonal development; thus, these three structures are considered equivalent to locomotor appendages from a morphological point of view. On the contrary, labrum and hypopharynx aren’t true appendages because of their non-metameric origin, although they are also considered buccal appendages due to their essential role in feeding.

What’s the function of each of these structures?

Knowing original functions of these structures on the mandibulate model lets us to understand the changes that have undergone the different adaptive forms emerged throughout the evolution of insects’ feeding:

Examples of mandibulate or chewing mouthparts: beetle (left) and locust (right). Source: John R. Meyer, North Carolina State University. Link.

• Labrum. A plate-like sclerite located before de rest of feeding structures, protecting them. Its size varies among species and it helps to contain the food. The posterior surface is known as epipharynx.
• Mandibles. A pair of jaws for crushing or grinding the food. They operate from side to side.
• Maxillae. A pair of appendages which are divided in three parts: cardo, which articulates with the head; stipes, which supports a sensory palp; galea and lacinia, which act as fork and spoon to manipulate the food.
• Hypopharynx. A little process located behind mandibles and between maxillae that helps mix food and saliva.
• Labium. Unlike mandibles and maxillae, the two original appendages forming the labium have fused together along the middle. The labium is also subdivided in two parts: postmentum, pieces which articulate with the head; prementum, distal pieces which support a pair of sensory palps and divide apically forming four lobes: glossae and paraglossae.

Mandible, maxilla, labium and hypopharynx (Davies, 1991).

Evolutionary adaptations of mouthparts

How did they evolve?

It’s considered that all models of mouthparts originally evolved from an ancestral mandibulate form. However, it’s more than probably that this process took place in different groups simultaneously when insects started to expand in range, food became more accessible and new sources of food appeared. This is an excellent example of adaptive radiation (when two or more populations, exposed to different selective pressures, diverge from a common ancestor).

Thanks to fossil records (insects preserved in amber, coprolites and evidences of attacks on plants) we know that the appearance of all models of mouthparts took place in at least 5 periods 420-110 myr ago. Eventually, some groups changed from a solid-based diet to a liquid-based diet: exposed liquids (e.g. nectar), tissue liquids (e.g. sap or blood) or even suspended particles. For those which adopted a liquid-based diet, these changes involved a great adaptive advantage during the expansion of angiosperms (flowered plants) in the Cretaceous period.

The adoption of a liquid-based diet by some insects, as the one seen in butterflies, involved a great adaptive advantage for these organisms during the expansion and diversification of flowering plants. Moreover, this gave room to the start of a coevolutive process between insects and plants. Author: Irene Lobato.

Types of mouthparts

On the basis of the mandibulate type, let’s see a summary of the main adaptive modifications observed in different types of mouthparts:

MANDIBULATE-LAPPING TYPE

Mandibulate-lapping mouthparts are linked to a liquid-based diet (e.g. nectar), even though in some cases they conserve the chewing function. They’re typical of hymenopterans. Sawflies or suborder Symphyta, considered the most ancient group of hymenopterans, conserve almost all original structures and functions of mandibulate mouthparts. Both wasps and bumblebees have undergone a reduction of both mandibles and maxillae and a massive development of labial glossae, forming a kind of tongue for drinking liquid food; however, they can still chew. Finally, bees have mandibles not for feeding, but for other purposes (such as fighting, grooming theirselves or working wax scales into honeycomb), and both maxillae and labial glossae lengthen giving room to a hairy tongue with an internal duct (the salivary duct), so their diet is exclusively liquid-based.

General scheme of lapping mouthparts of a bee (left; image by Xavier Vázquez, posteriorly modificated by Siga, CC) and mouthparts of a bee of the species Colletes willistoni (right; public domain image). Md: Mandibles; mx: Maxillae; lb: labium.

SUCKING-LAPPING TYPE

In this kind of mouthparts, mandibles undergo a massive reduction (and if present, they’re not for feeding purposes), even disappearing in some cases; so, insects with sucking-lapping mouthparts have a diet exclusively based on exposed liquids. There exist two main variations of this model: the ‘maxillar sucking’ or siphoning type typical of evolved lepidopterans and the ‘labial sucking’ or sponging type typical of flies and other dipterans.

In flies, mandibles are totally absent, maxillae are only represented by maxillary palps and posterior part of labium massively increase, forming two lobes which are sponge-like organs called the labella. The labella is a complex structure consisting of many grooves which sops up liquids much like a sponge does.

Sponging mouthparts of flies (left; source: Educational Media Group (EMG), RMIT University, 2002-06-01, Fly mouthparts illustration [Online, Image Illustration], Educational Media Group (EMG), Melbourne, Vic) and mouthparts of a fly of the species Gonia capitata (right; by Richard Bartz, CC).

In evolved lepidopterans, mandibles and labium are almost absent (only labial palps are visible), while maxillary galeae develop forming a long proboscis also known as ‘haustellum’ with a central alimentary duct for sucking liquids.

Siphoning mouthparts of a butterfly (left; by tdlucas5000, CC) and electron microscopy image of the proboscis (right; public domain image).

PIERCING-SUCKING TYPE

This type of mouthparts appears in different groups of insects with independent evolutionary lineages, so there exist lots of variations. Let’s see some examples:

• Heteroptera (bugs): they’re the only ones which possess this type of mouthparts since the very moment of birth. Both maxillary and labial palps are absent in these organisms, and labium forms a duct that encloses 4 stylets: two maxillary stylets and two mandibular stylets. This structures configure the beak or ‘rostrum’. Maxillary stylets delimit a salivary duct and a food duct, and together with mandibular ones allows the organism to pierce different tissues and then soak up their liquids: sap in phytophagous forms and blood in predatory ones.

Scheme of the piercing-sucking mouthparts of an heteropteran (left; image from Baker, 2011) and mouthparts of a predatory bug of the family Reduviidae (right; image property of John R. Meyer, North Carolina State University. Link).

• Mosquitoes: their mouthparts are very similar to the ones of bugs; however, they possess one more stylet, corresponding to the hypopharynx, which contains the salivary duct (through which they inject different substances to their hosts, such as anticoagulants). Labrum and hypopharynx together form the food duct, and labium has only an assistant function of supporting the stylets.

Scheme of mosquito’s mouthparts (left; by Xavier Vázquez, posteriorly modified by Siga, CC) and a mosquito female (right; by Grzegorz “Sculptoris” Krucke, CC). Lr: labrum; hp: hypopharynx; mx: maxillae; md: mandibles; lb: labium.

• Phthiraptera and Siphonaptera (lice and fleas): their mouthparts are formed by the epipharynx, both labial palps and both laciniae of maxillae. Maxillary palps are well developed and are always situated before the rest of the structure. Lice and fleas use their mouthparts to parasite their hosts, piercing their tissues and then sucking their blood.

Mouthparts of Siphonaptera (fleas): 1: eye; 2: labial palps; 3: maxillar stylet (lacinia); 4: hypopharynx; 5: maxillary palps; 6: maxilla (galea). Source: public domain.

• Thysanoptera (thrips): these tiny insects usually appear as pests in agricultural crops, sometimes even being vectors of different plant viruses. Their mouthparts present right-left asymmetry and the piercing structure is formed by the labium, the labrum and maxillae. Delimited by all these structures, there are also two maxillary stylets and only one mandibular stylet (the other one become atrophied). Thrips scratch the plant surface and then pierce it by their stylets, through which they suck plant fluids.

Scheme of thrips’ mouthparts (lefts; image form personal notes from the course “Biology and Diversity of Arthropods”, Universitat Autònoma de Barcelona) and frontal view of a thrip (right; property of John W. Dooley, USDA APHIS PPQ, Bugwood.org, CC).

AN EXTREME CASE: THE ATROPHY

Adult forms of some insects, such as mayflies (Ephemeroptera) or some dipterans, suffer a total reduction of their mouthparts. In these cases, the only function of adults is down to reproduction, so they lose all feeding functions and structures when metamorphose.

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There’s no doubt that insects form the most diverse group of organisms all over the world, showing not only a huge amount of species, but a big range of forms of mouthparts.

Do you know any other curious feeding structures in insects? Feel free to share your opinion or contributions in the comments. 

REFERENCES

• Agriculture and Life Science. General Entomology, NC State University.
• Blanke, A., Rühr, P. T., Mokso, R., Villanueva, P., Wilde, F., Stampanoni, M., … & Misof, B. (2015, August). Structural mouthpart interaction evolved already in the earliest lineages of insects. In Proc. R. Soc. B (Vol. 282, No. 1812, p. 20151033). The Royal Society.
• Davies, R.G. (1991). Introducción a la Entomología. Ed. MundiPrensa, Madrid.
• Grimaldi, D., & Engel, M. S. (2005). Evolution of the Insects. Cambridge University Press.
• Insect mouthparts. Amateur entomologists’ society.
• Krenn, H. W., & Aspöck, H. (2012). Form, function and evolution of the mouthparts of blood-feeding Arthropoda. Arthropod structure & development, 41(2), 101-118.
• Labandeira, C. C. (1997). Insect mouthparts: ascertaining the paleobiology of insect feeding strategies. Annual Review of Ecology and Systematics, 153-193.

There have also been consulted the personal notes taken from the subject “Biology and Diversity of Arthropods” given during the course 2013-2014 at the Universidad Autònoma de Barcelona.

Main photo, from left to right: 1) Lisa Brown, CC, 2) Public domain and 3) Richard Bartz, CC.