In the 1830s a German naturalist named Renous was arrested in San Fernando, Chile for heresy. His claim? He could turn caterpillars into butterflies. A few years later, Renous recounted his tale to Charles Darwin, who noted it in The Voyage of the Beagle.

Imprisoning someone for asserting what today qualifies as common knowledge might seem extreme, but metamorphosis—the process through which some animals abruptly transform their bodies after birth—has long inspired misunderstanding and mysticism. People have known since at least the time of ancient Egypt that worms and grubs develop into adult insects, but the evolution of insect metamorphosis remains a genuine biological mystery even today. Some scientists have proposed outlandish origin tales, such as Donald Williamson's idea that butterfly metamorphosis resulted from an ancient and accidental mating between two different species—one that wriggled along ground and one that flitted through the air.

Metamorphosis is a truly bizarre process, but an explanation of its evolution does not require such unsubstantiated theories (for a critique of Williamson's hypothesis, see this study). By combining evidence from the fossil record with studies on insect anatomy and development, biologists have established a plausible narrative about the origin of insect metamorphosis, which they continue to revise as new information surfaces. The earliest insects in Earth's history did not metamorphose; they hatched from eggs, essentially as miniature adults. Between 280 million and 300 million years ago, however, some insects began to mature a little differently—they hatched in forms that neither looked nor behaved like their adult versions. This shift proved remarkably beneficial: young and old insects were no longer competing for the same resources. Metamorphosis was so successful that, today, as many as 65 percent of all animal species on the planet are metamorphosing insects.

The egg of an idea
In 1651 English physician William Harvey published a book in which he proposed that caterpillars and other insect larvas were free-living embryos that abandoned nutrient-poor "imperfect eggs" before they matured. Harvey further argued that the cocoon or chrysalis a caterpillar entered during its pupal stage was a second egg in which the prematurely hatched embryo was born again. He entertained the idea that a caterpillar was one creature and a butterfly was an entirely different beast.

Some of Harvey's ideas were prescient, but he mostly misinterpreted what he observed. In 1669 Dutch biologist Jan Swammerdam rejected Harvey's notion of the pupa as an egg and the butterfly as a different animal than the caterpillar. Swammerdam dissected all kinds of insects under a microscope, confirming that the larva, pupa and adult insect were phases in the development of a single individual, not distinct creatures. He showed that one could find immature moth and butterfly body parts inside a larva, even before it spun a cocoon or formed a chrysalis. In some demonstrations, for example, Swammerdam peeled the skin off silkworms—the larval stage of the domesticated silk moth (Bombyx mori)—to reveal the rudimentary wings within.

Today, biologists know that these adult structures arise from clusters of cells called imaginal discs, which first form when an insect embryo develops in its egg. In some species, imaginal discs remain largely dormant until the pupal stage, during which they rapidly proliferate and grow into adult legs, wings and eyes, using dissolved larval cells as fuel and building blocks. In other species, imaginal discs begin to take the shape of adult body parts before the insect pupates (See Sidebar: How Does a Caterpillar Turn Into a Butterfly?)

Swammerdam also recognized that not all insects metamorphose in the same way. He proposed four kinds of metamorphosis, which biologists later distilled into three categories. Wingless ametabolous insects, such as silverfish and bristletails, undergo little or no metamorphosis. When they hatch from eggs, they already look like adults, albeit tiny ones, and simply grow larger over time through a series of molts in which they shed their exoskeletons. Hemimetaboly, or incomplete metamorphosis, describes insects such as cockroaches, grasshoppers and dragonflies that hatch as nymphs—miniature versions of their adult forms that gradually develop wings and functional genitals as they molt and grow. Holometaboly, or complete metamorphosis, refers to insects such as beetles, flies, butterflies, moths and bees, which hatch as wormlike larvae that eventually enter a quiescent pupal stage before emerging as adults that look nothing like the larvae. Insects may account for between 80 and 90 percent of all animal species, which means 45 to 60 percent of all animal species on the planet are insects that undergo complete metamorphosis according to one estimate. Clearly, this lifestyle has its advantages.

A new generation
Complete metamorphosis likely evolved out of incomplete metamorphosis. The oldest fossilized insects developed much like modern ametabolous and hemimetabolous insects—their young looked like adults. Fossils dating to 280 million years ago, however, record the emergence of a different developmental process. Around this time, some insects began to hatch from their eggs not as minuscule adults, but as wormlike critters with plump bodies and many tiny legs. In Illinois, for example, paleontologists unearthed a young insect that looks like a cross between a caterpillar and a cricket, with long hairs coating its body. It lived in a tropical environment and likely rummaged through leaf litter for food.

Biologists have not definitively determined how or why some insects began to hatch in a larval form, but Lynn Riddiford and James Truman, formerly of the University of Washington in Seattle, have constructed one of the most comprehensive theories. They point out that insects that mature through incomplete metamorphosis pass through a brief stage of life before becoming nymphs—the pro-nymphal stage, in which insects look and behave differently from their true nymphal forms. Some insects transition from pro-nymphs to nymphs while still in the egg; others remain pro-nymphs for anywhere from mere minutes to a few days after hatching.

Perhaps this pro-nymphal stage, Riddiford and Truman suggest, evolved into the larval stage of complete metamorphosis. Perhaps 280 million years ago, through a chance mutation, some pro-nymphs failed to absorb all the yolk in their eggs, leaving a precious resource unused. In response to this unfavorable situation, some pro-nymphs gained a new talent: the ability to actively feed, to slurp up the extra yolk, while still inside the egg. If such pro-nymphs emerged from their eggs before they reached the nymphal stage, they would have been able to continue feeding themselves in the outside world. Over the generations, these infant insects may have remained in a protracted pro-nymphal stage for longer and longer periods of time, growing wormier all the while and specializing in diets that differed from those of their adult selves—consuming fruits and leaves, rather than nectar or other smaller insects. Eventually these prepubescent pro-nymphs became full-fledged larvae that resembled modern caterpillars. In this way, the larval stage of complete metamorphosis corresponds to the pro-nymphal stage of incomplete metamorphosis. The pupal stage arose later as a kind of condensed nymphal phase that catapulted the wriggly larvae into their sexually active winged adult forms.

Some anatomical, hormonal and genetic evidence supports this evolutionary scenario. Anatomically, pro-nymphs have a fair amount in common with the larvas of insects that undergo complete metamorphosis: they both have soft bodies, lack scaly armor and possess immature nervous systems. A gene named broad is essential for the pupal stage of complete metamorphosis. If you knock out this gene, a caterpillar never forms a pupa and fails to become a butterfly. The same gene is important for molting during the nymphal stage of incomplete metamorphosis, corroborating the equivalence of nymph and pupa. Likewise, both pro-nymphs and larvae have high levels of juvenile hormone, which is known to suppress the development of adult features. In insects that undergo incomplete metamorphosis, levels of juvenile hormone dip before the pro-nymph molts into the nymph; in complete metamorphosis, however, juvenile hormone continues to flood the larva's body until just before it pupates. The evolution of incomplete metamorphosis into complete metamorphosis likely involved a genetic tweak that bathed the embryo in juvenile hormone sooner than usual and kept levels of the hormone high for an unusually long time.

31 Comments

1. 1. ACTORwriter 08:10 AM 8/10/12

   I put my money on either one of TWO advantages:
   1. It was/is a means of avoiding some predation.
   2. It was/is a better means of propagation.
   These are two of the most powerful evolutionarily successful mechanisms on the planet.

   Reply | Report Abuse | Link to this

2. 2. jtdwyer 09:06 AM 8/10/12

   Very interesting!
   How might the process of molting be related to metamorphosis?

   Reply | Report Abuse | Link to this

3. 3. Synoeca in reply to Gatnos 02:55 PM 8/10/12

   pfff. you lazy, breh.
   

   Reply | Report Abuse | Link to this

4. 4. ACTORwriter 03:31 PM 8/10/12

   What is truly embarrassing is the COMPLETELY unfounded [except by blind belief] of those who would accept such a foolish concept as "intelligent design". If ever there was a misnomer it is that term "intelligent" ... You have "INHERITED THE WIND", Gatnos. And the wind has blown from those who rely on ancient texts from superstitious generations of millennia ago. You would do yourself a favor by looking into the myriad bases of evidence which support the well-established theory of Evolution. You also give it away that you don't know what is meant in science by the term "theory". It's always better to find out what you don't know before you expose your ignorance in what you say.

   Reply | Report Abuse | Link to this

5. 5. Bill_Crofut 03:58 PM 8/10/12

   Re: "Perhaps this pro-nymphal stage, Riddiford and Truman suggest, evolved into the larval stage of complete metamorphosis. Perhaps 280 million years ago, through a chance mutation, some pro-nymphs failed to absorb all the yolk in their eggs, leaving a precious resource unused."
   
   Perhaps would seem to be an expression of caution. Yet, the process is touted as having been established as plausible based on the combined fossil evidence and subsequent studies.
   
   My understanding is that the vast majority of mutations is neutral at best, deleterious at worst. What is an example of a beneficial mutation which could have been responsible for metamorphosis?
   

   Reply | Report Abuse | Link to this

6. 6. Zexks in reply to Bill_Crofut 04:29 PM 8/10/12

   A mutation that prevented the juvenile hormones from being turned off early. While all the other bugs were growing to adult hood and competing for food, the mutant would still be a juvenile and without competition. The longer they wait to turn off those hormones the less competition they have for the resources they require.

   Reply | Report Abuse | Link to this

7. 7. marleysdaddy in reply to Bill_Crofut 04:31 PM 8/10/12

   "Perhaps would seem to be an expression of caution. Yet, the process is touted as having been established as plausible based on the combined fossil evidence and subsequent studies."
   
   That's how science works. Evidence and the results of research suggest likely mechanisms, until further evidence or different research provides more support for or overthrows those earlier ideas.

   Reply | Report Abuse | Link to this

8. 8. Zexks in reply to Gatnos 04:34 PM 8/10/12

   So not even gonna try and understand it, just "God did it" and that's it. How simple your world must be.

   Reply | Report Abuse | Link to this

9. 9. HowardB 05:11 PM 8/10/12

   Having read this article three times I see no 'explanation'. I simply see a series of observations tied together and set out as a broad rather vague theory.
   Now of course this is how Science works and it is perfectly acceptable as a vague theory. But SciAm is presenting is for what it is not. Metamorphosis is indeed a mysterious process and in my mind it remains a great mystery.
   "Ultimately, the impetus for many of life's astounding transformations also explains insect metamorphosis: survival."
   ALL evolution is driven by survival. This is a meaningless statement.
   "The primary advantage of complete metamorphosis is eliminating competition between the young and old. "
   As a theory this seems rather weak to me. It is also weak because there is no evidence for it. It is an interesting postulation, but that is all.

   Reply | Report Abuse | Link to this

10. 10. Ikpex 07:21 PM 8/10/12

    Observe the life cycle of Magicicadae to support this observation.

    Reply | Report Abuse | Link to this

11. 11. dylluvzjc 11:02 PM 8/10/12

    This is a very interesting article. Wow, 65% of all organisms are metamorphosing. Human is in the 35%. I just wonder if human do metamorphosis, perhaps alien-like? =D

    Reply | Report Abuse | Link to this

12. 12. elderlybloke 12:59 AM 8/11/12

    Gatnos ,
    There is one good thing about your belief, it avoids that difficult thing called thinking.

    Reply | Report Abuse | Link to this

13. 13. Bill_Crofut 11:38 AM 8/11/12

    Zexks (comment 7),
    
    Has any researcher identified the mutation?

    Reply | Report Abuse | Link to this

14. 14. Bill_Crofut 11:38 AM 8/11/12

    marleysdaddy (comment 8),
    
    It's quite clear how the brand of science presented on this web page works. Assertions (i.e., "evidence from the fossil record with studies on insect anatomy and development") have been presented as positive arguments. What fossil evidence combined with what subsequent studies have made the assertions plausible?

    Reply | Report Abuse | Link to this

15. 15. jtdwyer 02:29 PM 8/11/12

    This is an article presenting a hypothesis that is supported by a research report published under the heading "Hypothesis" in a peer reviewed scientific publication, referenced in this article:
    James W. Truman & Lynn M. Riddiford, (1999), "The origins of insect metamorphosis",
    http://www.nature.com/nature/journal/v401/n6752abs/401447a0.html
    
    Also see the referenced freely available open access research report:
    Deniz F. Erezyilmaz, (2006), "Imperfect eggs and oviform nymphs: a history of ideas about the origins of insect metamorphosis",
    http://intl-icb.oxfordjournals.org/content/46/6/795.full

    Reply | Report Abuse | Link to this

16. 16. HowardB in reply to jtdwyer 02:53 PM 8/11/12

    Your first reference is broken - but your second is interesting, though 6 years old, and makes me wonder why it was not referenced in the article above ?

    Reply | Report Abuse | Link to this

17. 17. HowardB in reply to Bill_Crofut 02:57 PM 8/11/12

    I agree. No references to any evidence to support his article and a thoroughly subjective piece of journalism.
    His dismissive attitude to Donald Williamson's idea as "outlandish" is really quite appalling considering we are discussing metamorphosis, an outlandish biological process in and of itself ...
    Regrettably this is part of the general trend in SciAm which has drifted away from Science and into the world of the tabloid more and more in recent years.

    Reply | Report Abuse | Link to this

18. 18. jtdwyer in reply to HowardB 04:58 PM 8/11/12

    Thanks for pointing out my error. This should be the correct link (with the missing slash):
    http://www.nature.com/nature/journal/v401/n6752/abs/401447a0.html
    
    Actually, both research reports are referenced by dynamic links within this article; the first near the beginning of para. 2 under the heading "A new generation" ("... constructed one of the most comprehensive theories"); the second in the forth para. under the same heading ("... supports this evolutionary scenario").

    Reply | Report Abuse | Link to this

19. 19. ridelo 05:12 PM 8/11/12

    "It is an interesting postulation, but that is all."
    So now, sleeves up and searching for more evidence. They have shown that metamorphosis could enhance survival. I find that very convincing, for the time being. I'm waiting for somebody who can falsify this.

    Reply | Report Abuse | Link to this

20. 20. Bill_Crofut 07:23 PM 8/11/12

    jtdwyer (comment 16),
    
    Re: http://www.nature.com/nature/journal/v401/n6752abs/401447a0.html
    
    Entering that url resulted in the following message:
    
    Error: page not found
    
    You might not be able to find the page you are looking for because of an out of date bookmark/favourite, or possibly a mis-typed address (in which case it may be worth trying again).
    
    If retyping the address still doesn't work, try using our search to find the page you want. Alternatively browse our sites using the list below:
    
    That, in itself, is not of any particular concern. My experience has been the online copies of papers from NATURE are only available to me at unacceptable cost.
    
    Re: http://intl-icb.oxfordjournals.org/content/46/6/795.full
    
    A cursory review of this paper indicates it's nothing more than a history lesson. Is there anything in particular on which you would like me to focus?
    

    Reply | Report Abuse | Link to this

21. 21. Bill_Crofut 07:24 PM 8/11/12

    HowardB (comment 18),
    
    My guess is, Donald Williamson's proposal is no more acceptable to me than any of the other proposals thus far presented.
    

    Reply | Report Abuse | Link to this

22. 22. jtdwyer in reply to Bill_Crofut 07:57 PM 8/11/12

    No, I've got nothing in particular or in general to present or propose to you - certainly nothing that could possibly be acceptable to you.

    Reply | Report Abuse | Link to this

23. 23. Andrew Planet 09:32 PM 8/11/12

    Metamorphosis. The adaptation in ability to build an organic scaffolding in different forms of complexity unfolding in growth as in origami

    Reply | Report Abuse | Link to this

24. 24. HowardB in reply to jtdwyer 11:36 AM 8/12/12

    "Actually, both research reports are referenced by dynamic links within this article"
    
    You are correct. My error. However I remain critical because I find this dynamic reference habit inadequate. An article should have it's academic references at the end of the article or explicitly stated within the article. Dynamic links are fine with background information or other SciAm articles. That is how I see it anyway.

    Reply | Report Abuse | Link to this

25. 25. HowardB 11:39 AM 8/12/12

    20. ridelo:
    "So now, sleeves up and searching for more evidence. They have shown that metamorphosis could enhance survival. I find that very convincing, for the time being. I'm waiting for somebody who can falsify this."
    
    That is fine ! that is how Science works. But you don't make an announcement that the explanation has been found, which is the implication of the article headline.

    Reply | Report Abuse | Link to this

26. 26. jtdwyer in reply to HowardB 03:02 PM 8/12/12

    IMO, you're being overly critical here. The title simply asks the question without making any proclamations. The subtitle states that "metamorphosis remains somewhat mysterious" but adds, "biologists have gathered enough evidence to _plausibly_ explain..." This hardly seems to be a definitive announcement, but one appropriate for a fairly recent hypothesis that, after several years has not been denounced by peer review.
    
    I certainly agree the SA is often guilty of overstatement and hyperbole, especially in their titles, but this case seems appropriately stated to me...

    Reply | Report Abuse | Link to this

27. 27. jtdwyer in reply to jtdwyer 03:10 PM 8/12/12

    That being said, looking back at the article link caption on the SA home page: "Origin of Insect Metamorphosis Explained" - I wholeheartedly agree with your assessment!

    Reply | Report Abuse | Link to this

28. 28. HowardB in reply to jtdwyer 03:43 PM 8/12/12

    27. jtdwyer
    
    I do take your point about being over critical. I guess I expect a bit more from SciAm than from the NYT or from a tabloid reporting on Science.
    I also think this Metamorphosis thing is an absolutely fascinating process, and a prime topic for an extended section in SciAm

    Reply | Report Abuse | Link to this

29. 29. DiJiT in reply to ACTORwriter 05:38 PM 8/12/12

    "Larval insects and adult insects occupy very different ecological niches. "
    
    Couldn't the same be said for human children who have a more delayed maturation? Or, do insects that undergo metamorphosis lead more complex adult lives--genetic memory is preserved with this type of growth (butterflies). Again, somewhat similar to human children who develop more complex brains.

    Reply | Report Abuse | Link to this

30. 30. jtdwyer in reply to HowardB 07:08 PM 8/12/12

    I agree - an excellent suggestion!

    Reply | Report Abuse | Link to this

31. 31. Andrew Planet 04:07 PM 8/20/12

    The adaptation in ability for building an organic scaffolding in different forms of complexity unfolding in growth as in origami.

    Reply | Report Abuse | Link to this