"Hopeful Monsters", Saltationism, and Other Useful Ideas in Evolutionary Theory

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The concept of "hopeful monsters" in evolutionary theory has a storied and somewhat controversial history. Coined by German geneticist Richard Goldschmidt in the early 20th century, the term refers to the idea that large, sudden mutations could produce entirely new species in a single generation—a radical departure from the gradualist perspective that dominated evolutionary thought at the time. Goldschmidt's ideas were largely inspired by his work on the gypsy moth, where he observed significant morphological changes that could not be easily explained by small, incremental mutations.

During Goldschmidt's era, the prevailing view was that of gradualism, heavily influenced by Charles Darwin's "On the Origin of Species." According to this view, evolution occurred through the slow accumulation of small changes in features, each conferring a slight advantage or disadvantage, and then being subject to natural selection over long periods. Goldschmidt's "hopeful monster" hypothesis was met with skepticism and even ridicule, as it seemed to echo the outdated, pre-Darwinian ideas of "saltationism," where new species would leap into existence, an idea similar to the concept of spontaneous creation.

The discovery of the structure of DNA and the advent of molecular biology in the mid-20th century brought new perspectives. With a better understanding of genetics, researchers began to see how, in addition to regular-occurring small mutations, large mutations at key developmental genes, sometimes called "master control genes," could indeed result in significant morphological changes. These ideas, which revealed highly coordinated, coadapted regulatory networks, were further supported by the emerging field of evolutionary developmental biology, or "evo-devo," which studies how developmental processes contribute to evolutionary change.

Variation in hox genes is related to the diversity of forms found in molluscs. Adapted from Salamance-Diaz, Nature Scientific Reports, 2021.

Still, these new data suggested that evolutionary tendencies toward major shifts in biological morphology and physiology might come up against evolutionary constraints: the more complex and integrated an aspect of biology, it was thought, the less likely the wholescale reformation space that might be possible, limiting the emergence of “hopeful monsters” within certain lineages on the tree of life.

Exceptions Prove Rules in Evolution

But that actually helps make the point: atrocities such as animals that can walk on slick, vertical surfaces, or others that can glide on slime across a bed of leaves or walk sideways might be rare because their kind cannot easily break the regulatory networks of the past, and thus their unusual biology that makes them aberrations. They are uncommon evolutionary novelties, which might make them rare. And to us, those who have inherited the ability to survey the vast tapestry of life, living and extinct, rare is usually interpreted as “improbable”. Could gradual evolution be interspersed with occasional new forms due to evolutionary constraints? Could macromutations be common, but large shifts occur rarely due to the rarity of the co-occurrence of the right monster in the right environment?

Much of the fossil record would seem to align with this idea. In the late 20th and early 21st centuries, the concept of "hopeful monsters" experienced a sort of renaissance, albeit under different terminologies and frameworks. Scientists Stephen Jay Gould and Niles Eldredge, who advocated for the theory of "punctuated equilibrium," argued that evolutionary change might not always be gradual and could occur in fits and starts. This was somewhat vindicated by the discovery of "key innovations" in the fossil record—traits that opened up new ecological niches and led to rapid speciation. (See images modeling gradualism punctuated equilibrium, and episodic evolution by Judge Starling — (Illustrating Punctuated Equilibria, Phyletic... (tumblr.com)).

Key innovations often cited include the hypocone - the inner cusp of mammals - a specialized trait that allows herbivory. Adhesive toepads in lizards, while remarkably innovative, might not fall into the category of “monsters”, either, but rather can now be understood as resulting from add-ons to, not disruption of, the developmental programming that controls scale development. The recurring appearance of de novo adhesive toepads also means that the trait may be relatively easy to come by (See Convergent Developmental Patterns Underlie the Repeated Evolution of Adhesive Toe Pads Among Lizards (marquette.edu)). The same is true for floral nectar spurs on the flowers of some angiosperms.

Most of the often-cited examples key innovations seem to fall short of qualifying as hopeful monsters. Others that are more truly monstrous, in my opinion at least, are organisms that keep evolving into crabs. This tendency is so frequent it has its own name: carcinization. Here, you have many instances in which a perfectly good crustacean or arthropod lineage that moves forwards and maybe backwards due to encephalization discovers efficiency in moving in an expected manner. In fact, crabs and crab-like organisms not only have unexpected behaviors; they have unexpected shapes and, due their vector of locomotion, unexpected locations of sensitive eyes and defense weapons. Not unexpected by us; unexpected by their competitors, and natural foes: their predators. Horrific creatures like young, inexperienced crab plovers, great egrets, tufted ducks, sea gulls, and ruddy turnstones might underestimate their pluck and aim for where they expect the crab might be, instead of jabbing in the waves where the crab will be, as they learn to do better as they age.

Could carcinization be an adaptive anti-predation strategy? Or a strategy to withstand the undertow of breaking waves? Or both?

Lancelot Alexander Borradaile first coined the term carcinization in 1916, which he described as follows:

“... carcinization … consists essentially in a reduction of the abdomen of a macrurous crustacean, together with a depression and broadening of its cephalothorax, so that the animal assumes the general habit of body of a crab”

A very neat study of the distribution of crab-like features found that there were multiple ways to become a crab if you’re a crustacean. (See: How does a crustacean become a crab? | EurekAlert!) and How to become a crab: Phenotypic constraints on a recurring body plan (wiley.com).

Phylogenetic evidence from Ms. Joanna Wolfe and her colleagues’s previous work demonstrates that carcinized body plans have evolved multiple times - and in distinct configurations, as indicated by the colored characteristics on branches. (IMAGE CREDIT: Courtesy of Joanna M. Wolfe.)

Today, while the term "hopeful monsters" is rarely used in scientific discourse, the idea that large mutations can sometimes result in significant evolutionary leaps is not entirely dismissed. It has found a more nuanced expression in modern theories that integrate genetics, development, and paleontology. For example, the study of "adaptive radiations," where a single ancestral species rapidly diversifies into multiple new forms, often involves mechanisms that could be considered 'hopeful monster' under certain conditions.

As monstrous as a crab may appear to us, morphologically, it’s just another crustacean. Sure, it’s lost its tail. But that’s a trick: true crabs tails are actually neatly tucked under their bodies. Among all major animal groups, the molluscs impress me most with their predilection to and success at evolving into monsters. First, unlike anything we see today, the likely ancestor of all molluscs was a flat worm-like invertebrate (something like an Aplacophoran) one of which, for some reason, had a shell on its head and on its anterior part. These shells were destined to become the shells of shellfish. Consider the lowly clam… having lost its head, and for all purposes that we can recognize, also having lost organized segmentedness, are a breed apart in animals. If no other molluscs survived to modern times, they would be a lonely outlier among animals. A squishy mess with an approximation of being an animal.

However, they are not alone; the entire, wildly diverse molluscan lineage lost the coordination of the entire body plan via a reshuffling of the regulation of the expression of their hox genes, one of the most remarkable monster-generating things that could possibly happen to an animal lineage. (See: Non-collinear Hox gene expression in bivalves and the evolution of morphological novelties in mollusks.)

Clams. (Shutterstock)

Hox genes are spatially organized regulatory genes in vertebrates and segmented invertebrates whose timing of expression is key to the development of genomically programmed body plans. You have the number of vertebrae and each is in place where it should be because your hox genes told your body to make that many, there. Insects have their thorax, abdomen, and head where they are because their hox genes gave them this order. Centipedes, and millepedes, all have the number of legs they do, in the order they do, and their head where it should be, because of their hox genes.

A giant tree centipede (Shutterstock)

But this layer of organization - repeated patterns enforced by rigid control of the timing and amount of the expression of genes in key developmental programs - also means that you’re not likely to evolve a monster. This idea that the evolution of complexity constrains evolution has also been very recently published as having the effect of less biodiversity due to a restricted range of niches available for a given bauplan to explore, in birds, for example (See Phys.org: Study shows birds that have evolved greater complexity are less biodiverse).

Helix promatia, a somewhat organized garden snail having a summer day in the garden. (Shutterstock)

It was the disruption of the genomic coordination of the hox genes which has allowed molluscs to evolve into the most anatomically and confusing animal group that we have, which includes snails and slugs (Gastropods), clams and their kin (Bivalvia), horn-like creatures that have apparently no other relatives (Scaphopoda), octopi and their relatives (Cephalopoda), all related to and nested within segmented organisms and obscure barely noticeable lesser-known animals like the Polyplacaphora (marine molluscs), Chaetodermomorpha (worm-like and yet not worms). And last, but not least, the Neomeniomorpha - wormlike yet not worms with no sign of a shell, mantle or other bony organ used so diversely by the rest of the molluscs. They are a living plug. As animals go, molluscs are all over the evolutionary map.

At times, when I’m teaching The Principles of Evolutionary Biology, I always try to remember some of the most interesting things I’ve learned while studying evolution and reading about studies conducted by evolutionary biologists and theorists. In all of the great story of the evolution of biodiversity on earth, the clade of animals that strike me as the most likely place to find hopeful monsters is, indeed, the molluscs. They are the unsung heroes of animal evolution.

For me, thanks in large part to my molluscan friends, the concept of "hopeful monsters" has evolved from being a scientific heresy to a topic of nuanced discussion that incorporates complex genetic and developmental mechanisms. While not fully embraced by evolutionary biologists in its original form, the essence of the idea continues to challenge and enrich our understanding of how life evolves, offering a more pluralistic view of evolutionary mechanisms.

I’m not a vegetarian, but I no longer eat Cephalopods. I have deep fondness and respect for the consciousness in cephalopods. There are more than a few interesting pieces of writing. Other Minds by Peter Godfrey-Smith was a treat, and actually represents fairly well part of a book I’ve been wanting to write for ten years. My Octopus Teacher is a wonderful documentary and a very nice place to begin to ponder the experiences of a cephalopod.

A cuttlefish (Sepia officinalis) underwater in a bed of sea lettuce (Shutterstock)

We Could Only Hope to Be Monsters

What about us? Homo sapiens? Morphologically, in the evolution of our own species, our extinct relatives experienced lineage-specific variation in the amount of variance (amount of change) in the bone anatomy of the skull. This variation over time was studied by Rocatti and Perez (published in 2019), who, using the age-old methodology of morphometrics, combined with modern statistical analyses, found that of the hominin lineages that experimented the most with skull shape, individual lineages surpassed general larger phylogenetic groups of lineages.

The uniformity of our skulls across our species reflects recent shared common ancestry and high amounts of gene flow. The evolutionary experiments reflected by the higher morphometric variance found by Rocattis and Perez means that there have been some outliers in regard to skull shape evolution during the evolution of ourselves and our extinct ancestors over the last 10 million years (See: The Evolutionary Radiation of Hominids: a Phylogenetic Comparative Study)

Who knows? Maybe to some future invertebrate sentient paleontologist, we might appear to have been hopeful monsters compared to their own viewpoints on evolution.

Toumaï fossil, still debated by upright apes as either being an frequently unright ape, or hominin. Wikimedia (IMAGE CREDIT: Didier Descouens/Wikimedia Commons). (Wikipedia Article)

Citations

Brinkworth et al, Bird clades with less complex appendicular skeletons tend to have higher species richness, Nature Communications (2023). DOI: 10.1038/s41467-023-41415-2 Journal information: Nature Communications

Eldredge, N. & Gould, S.J. Punctuated equilibria: an alternative to phyletic gradualism (1972) pp 82-115 in "Models in paleobiology", edited by Schopf, TJM Freeman, Cooper & Co, San Francisco. https://www.blackwellpublishing.com/ridley/classictexts/eldredge.asp

Rocatti & Perez, 2019. The Evolutionary Radiation of Hominids: a Phylogenetic Comparative Study 9:15267 https://www.nature.com/articles/s41598-019-51685-w

Salamanca-Diaz, et al. Non-collinear Hox gene expression in bivalves and the evolution of morphological novelties in mollusks. Nature Scientific Reports 11 Feb 2021. 11:3575 https://www.nature.com/articles/s41598-021-82122-6

Wolfe JM, Luque J, Bracken-Grissom HD. How to become a crab: Phenotypic constraints on a recurring body plan. Bioessays. 2021 May;43(5):e2100020. doi: 10.1002/bies.202100020. Epub 2021 Mar 9. PMID: 33751651.