Double lives: the evolution of insect metamorphosis

I found these the other day. Cute or what?!

True, most people prefer the adult version- particularly if turns out to be a butterfly. Caterpillars almost seem like different species when they grow up- their bodies change beyond recognition, as do their lifestyles. This type of life cycle is called holometabolism, in which a soft-bodied eating-machine of a larva forms a pupa at the end of its growth. Here, it undergoes a staggering transformation to become an adult: a change commonly known as metamorphosis. All “Very Hungry Caterpillar” so far. But butterflies and moths shouldn’t get all the limelight. In fact, the larvae in my photo above aren’t caterpillars at all: they’re young Hazel Sawflies, relatives of bees, wasps and ants. About 80% of all insect species are thought to adopt this life cycle, including the aforementioned bees and their relatives, beetles, and flies.

Most of the remaining insect species have a much OLDER method of growing up: the young insects basically resemble small versions of their parents, with hard exoskeletons and, frequently, similar lifestyles to the adult. These youngsters are often known as “nymphs”. Like holometabolous insects, they shed their skins as they grow, separating their youth into multiple “instars”. When they moult out of their skins for the final time, they emerge as adults: the only major features gained in this final transformation are wings and functional genitalia. Grasshoppers, true bugs and dragonflies are good examples of this fast-track hemimetabolous lifestyle.

I've spent a lot of time cooing over insects in my last few posts. N'AWWW!

For a long time, it was assumed that the larvae of holometabolous insects were equivalent to hemimetabolous nymphs, and had simply become highly specialised over evolutionary time. Genetics tell us that all holometabolous insects had a common ancestor: i.e. this lifestyle has only evolved from hemimetabolism ONCE. But how and why they evolved so many differences- the soft body, the complicated pupal stage- was a bit of a mystery. It’s hard to imagine a fully-formed nymph, just a few simple developmental steps away from being a functional adult, being selected to gradually become more and more like a soft sack of guts. Eventually, the differences between baby and adult would be so great that only liquidising the larva in a stationary, vulnerable pupa could produce the necessary change to its body: it just makes growing up complicated! And how did they insert this new life-stage into their development from nowhere?

Then, in 1999, Truman and Riddiford cracked the metamorphosis puzzle. They noticed that in hemimetabolous insects, there was actually ANOTHER, very short, developmental stage in between the embryo in the egg and the nymph! Before moulting into a true nymph, this “pronymph” has a soft body, no wing buds, unusual bodily proportions and an underdeveloped sensory system: features also seen in holometabolous larvae. Is this, in fact, the stage that gave rise to caterpillars and maggots? But the pronymph cannot feed, as its mouthparts are also soft: what pressures could possibly have led to the extension of this brief, rather vulnerable phase?

Truman and Riddiford ask us to imagine a mutant hemimetabolous insect that starts leaving a small pocket of yolk inside its eggs: something that modern butterflies and moths also do. This food source is wasted upon an embryo that cannot feed, but if a pronymph were to develop the ability to eat the yolk whilst in the egg, it would have a great advantage- a pre-hatch snack to prepare it for the challenges of the outside world! Early development of nymphal features like hard mouthparts can be induced by playing around with the hormones of modern pronymphs in the egg, showing us a possible mechanism for this anomaly.

 Like many modern insects, this ancestral insect may have laid its eggs in the soil or in some other secluded environment, away from danger. Therefore, the pronymphs may have had to burrow out of their birthplace before their first moult into a nymph. But the feeding pronymph would have seen things a little differently:  there was food here! Perhaps it was decaying wood under the bark where it hatched (which many young beetles feed on today), or plant roots in the soil. Either way, it was inaccessible to other members of its species: adults and nymphs rarely found themselves in this environment, and other pronymphs were simply unable to eat it. So as well as a head-start from their eggy breakfast, mutant pronymphs also got a boost from helping themselves to some abundant food source for which there was no competition. The advantages of exploiting this resource may have been so great that in future generations, it was better to put off becoming a true nymph, and hold on to pronymph characteristics even after moulting. Gradually, the pronymph stage would have become more and more extensive, and more and more specialised for eating the new food source. This meant the normal nymphal development had to be compressed into a much shorter, more intense period. That’s right- the pupa. This putative sequence of events is much more elegant- we no longer have to explain how nymphs regressed from mini-adults to bizarre eating machines, or how the pupal stage arose de novo. As in countless cases, evolution has tweaked with already-existing material rather than starting from scratch, eventually changing  some features of the organism beyond recognition.

Today, holometabolous insects continue to reap the benefits of their dramatic coming-of-age. Adults and larvae live such different lifestyles that they don’t compete for food and space- leading to a higher population- and a single species can become perfectly adapted to multiple ecological niches. In fact, the latter point could even explain why holometabolous insects are so diverse: living in two different environments might mean encountering twice the amount of environmental change over time. Adaptation to this change, or innovations that allow a new niche to be taken on by one life-stage, means more chance of a new species arising. Some non-metamorphic species- like dragonflies, whose larvae live underwater- have managed some level of ecological separation, but it’s nothing compared to the bizarre rift between the amorphous maggot and its highly-structured parent.

So, next time we ponder over the huge differences that make caterpillars and butterflies seem like entirely separate species, we should remember:  that’s kind of the whole point!

Image credits: Grasshopper nymph by Obsidian Soul (Own work) [CC-BY-SA-3.0 (http://creativecommons.org/licenses/by-sa/3.0) or GFDL (http://www.gnu.org/copyleft/fdl.html)], via Wikimedia Commons