Darwin and Fishes

by Dr. Warren Allmon

First posted February 6, 2023

Charles Darwin is of course known as the founder of the modern science of evolution. It is unfortunately less widely appreciated how many other scientific fields he contributed to, or even founded. Indeed, the scope of his scientific work is astonishing. His most substantial early scientific contributions were in geology, including books on the geology of South America, volcanic islands, and the formation of coral reefs. Before publishing On the Origin of Species, Darwin spent eight years studying the taxonomy of barnacles, and published three books of the results. After the Origin, he devoted much of his time to botany, and published six books on plants. The last of his books was about earthworms. He invented the scientific study of animal behavior, the concept of sexual selection, and the application of natural science to explaining the origin and characteristics of human beings. He was a zoologist, ecologist, paleontologist, anthropologist, and entomologist.[1]

In other words, Darwin was the consummate naturalist, interested in every part of the natural world, including fishes. Although he did not publish any books or scholarly papers specifically on fishes, he collected, studied, and used fishes of many kinds as evidence and examples of evolution and natural selection. He puzzled over possible evolutionary explanations of peculiarities of fish biology, and pondered the significance of modern lungfishes, which were first described by other scientists early in Darwin’s career, for the evolution of limbed land vertebrates.[2]

Before the Beagle

The young Darwin is well-known as a beetle collector, but he was also an avid angler, and careful reader of Izack Walton’s famous book on fishing, The Compleat Angler, first published in 1653. As ichthyologist Daniel Pauly notes, “Walton’s classic, which identifies (and names!) distinct populations of Trout and other fish species in the British Isles, may have contributed, a decade or so later, to [Darwin’s] dawning perception of within-species variation as a motor of evolution”[3]. “I had a strong taste for angling,” wrote Darwin in his Autobiography, “and would sit for any number of hours on the bank of a river or pond watching the float.”[4]

Darwin’s earliest known scientific writing is a notebook entry from March 16, 1827 concerning the dissection of a lumpfish (Cyclopterus lumpus) conducted under the guidance of his mentor Robert Grant in Edinburgh during Darwin’s brief residence there as a medical student.[5]

Darwin’s Beagle Fishes

Darwin collected many specimens of fishes during the Beagle voyage (December 27, 1831 - October 2, 1836). Like all his voluminous collections, these were shipped back to England. Upon his return, Darwin organized the distribution of the specimens to various specialists who, he hoped, would identify and describe them in detail.[6] The fishes were entrusted to naturalist and clergyman Leonard Jenyns (1800-1893), who described and published them in the Zoology of the Voyage of H.M.S. Beagle, which Darwin edited, in 1840-41. Jenyns and Darwin had met through Darwin’s Cambridge mentor John Stephens Henslow, who married Jenyns’ sister. The fish specimens were originally placed in the Museum of Zoology at Cambridge, where they remained until 1917, when most were transferred to the Natural History Museum in London. At least 164 specimens, representing 137 species, remain in these two museum collections today according to their catalogs.

One of the most notable features of living fishes is their color. Darwin the careful naturalist knew that color would fade from fish specimens stored in preservative, and so during the voyage he made careful notes about their colors when fresh, basing these descriptions on color-coded charts in a book he brought along with him for that purpose. Thus, writes Pauly, “we can attribute to [Darwin] the first rigorous treatment of colours in biology in general, and in ichthyology in particular”[7].

In his Diary and the published Voyage of the Beagle, Darwin included several detailed descriptions of the behavior of fishes, e.g., Diodon, the porcupine fish:

One day I was amused by watching the habits of a Diodon, which was caught swimming near the shore. This fish is well known to possess the singular power of distending itself into a nearly spherical form. After having been taken out of water for a short time, and then again immersed in it, a considerable quantity both of water and air was absorbed by the mouth, and perhaps likewise by the branchial apertures. This process is effected by two methods; the air is swallowed, and is then forced into the cavity of the body, its return being prevented by a muscular contraction which is externally visible; but the water, I observed, entered in a stream through the mouth, which was wide open and motionless: this latter action must, therefore, depend on suction. The skin about the abdomen is much looser than that of the back; hence, during the inflation, the lower surface becomes far more distended than the upper; and the fish, in consequence, floats with its back downwards.[8] 

Fishes in the Origin and Beyond

Darwin used fishes as abundant sources of questions, examples, and evidence about evolution throughout On the Origin of Species and in his unpublished writing.

For instance, he puzzled about the causes for bright or shiny coloration in fishes, noting that non-evolutionary thinkers had argued that such fishes were conspicuous so that they could be caught by predators[9]. Darwin explained some of these patterns as a result of sexual selection (which he proposed in Descent of Man, 1871). He also noted that many fishes bear structures only in the males, such as barbels on their jaws or crests on the heads, that are difficult to explain except by sexual selection.

Darwin was also interested in differences between marine and freshwater fishes, mainly because he was concerned about anything that could affect the geographic distribution of species. Geography was central to Darwin’s thinking about evolution. The very first sentence of the Origin makes this clear: “When on board H.M.S. ‘Beagle,’ as naturalist, I was much struck with certain facts in the distribution of the inhabitants of South America…”[10]. Where species occurred in space was a record of what had happened to them through time. Species moving from place to place put them into new habitats, isolated from other populations, and so set up conditions that might allow evolutionary change to occur. The movement of fishes between salt and fresh water was therefore an important process to understand. Darwin carried out extensive experiments to test the ability of fishes to withstand rapid changes of salinity so that he could assess their ability to move between marine and freshwater habitats and thereby increase their range[11]. Not only were fishes of interest for their own sake, but also as potential vectors for the movement of plants via their seeds. Darwin studied whether fish would eat particular seeds, and if so whether those seeds would germinate once they had passed through the gut, or once the fish had passed through the gut of a bird. In the Origin, he wrote: “Freshwater fish, I find, eat seeds of many land and water plants: fish are frequently devoured by birds, and thus the seeds might be transported from place to place.”[12]

Darwin was also fascinated by goldfish, which are the domesticated and highly modified descendants of several species of Asian carp, the result of more than 800 years of artificial selection by Chinese breeders. In writing at length about this in The variation of animals and plants under domestication (1868), he observes that “the goldfish, from being reared in small vessels, and from having been carefully attended to by the Chinese, has yielded many races”[13].

Electric fishes were also of great interest to Darwin. He noted that electric organs occur in fishes that are clearly not closely related, and he cited this as a clear example of convergent evolution[14].

One of the most familiar examples of evolution in popular culture today is the transition from “fishes” to “amphibians,” an event that paleontologists and evolutionary biologists refer to as “the origin of tetrapods” or “limbs from fins.” The origin of four-legged land vertebrates was of great interest to Darwin. Living lungfishes had only been recently discovered when Darwin began seriously thinking about evolution. These distinctive animals inhabit freshwaters in Australia, South America, and Africa. When the habitats of African lungfishes dry out, they burrow into the mud, form a cocoon of mucus around their body, and aestivate until wet conditions return[15]. British anatomist Richard Owen described the African lungfish Protopterus annectens in 1839. When he described it in 1837, Leopold Fitzinger thought the South American lungfish Lepidosiren paradoxa was an amphibian, hence his name for it which means “scaly siren.” (The Australian lungfish Neoceratodus forsteri was described in 1870 by Johann Ludwig Gerard Krefft, about fifty years after Devonian fossil toothplates like those of Neoceratodus were described.) Darwin frequently used the African species (which he referred to as Lepidosiren annectens) to represent lungfishes in general, and as a transitional form between fishes and tetrapods: “it would not be ridiculous to suppose that the Lepidosiren could be modified by natural selection into an ordinary fish, or into a reptile”[16]. Darwin also noted that lungfishes – which differ so strongly from other fishes, appear to have lost structures more fully developed in their ancestors: the limbs of Lepidosiren, Darwin argued, “are probably remnants, consisting of the persistent axis of a fin, with the lateral rays or branches aborted.”[17]

Flatfishes

One of Darwin’s most interesting and extensive explorations of fish evolution had to do with “flatfishes,” the group of mostly marine fishes that includes familiar food species such as haddock, sole, and flounder. These unusual fishes are characterized by profound asymmetry of their heads, resulting from the migration of one eye to the opposite side of the skull during larval metamorphosis. This extreme change during development allows adult flatfishes to rest on the seafloor on their eyeless side. Darwin was motivated to dive into this distinctive group by one of his most articulate critics, British biologist St. George Jackson Mivart (1827-1900).

In 1871, Mivart published a book-length attack on Darwinian natural selection entitled On the Genesis of Species. Mivart’s essential criticism was that natural selection could not be the creative force that Darwin demanded. How, asked Mivart, was it possible for highly complex features – such as a bird’s wing or the vertebrate eye – to evolve gradually by natural selection? Such features, Mivart argued, could not accomplish their function until they were complete, and so the incomplete precursor stages could not be selected for. He called this problem “the incipient stages of useful structures.” One of Mivart’s examples was the peculiar form of flatfishes. Such a condition, argued Mivart, could not have been achieved by any gradual process of selection of slight variants such as Darwin proposed:

“…the accidental occurrence of such a spontaneous transformation is hardly conceivable. But if this is not so, if the transit was gradual, how such transit of one eye a minute fraction of the journey towards the other side of the head could benefit the individual is indeed far from clear. It seems, even, that such an incipient transformation must rather have been injurious.”[18]

Darwin’s general response to the “incipient stages” challenge was to point out that there was no requirement in his theory that every feature must be built by natural selection for its current function. On the contrary, Darwin argued that the initial stages of many complex features may well have been selected for partly or completely different functions than those that they now serve. Early stages of wings, for example, may have served as airfoils to assist jumping off the ground, and the first stages of eyes may have been functional as light-detecting organs long before they formed clear images. Darwin’s explanation is universally accepted by evolutionary biologists today.

In the case of cranial asymmetry in flatfishes, however, Darwin also applied an argument that we reject today: the inheritance of acquired characteristics, commonly known as “Lamarckian inheritance” after French naturalist Jean-Baptiste Lamarck (1744-1829), who championed the idea in the early nineteenth century. Darwin wrote in the fifth edition of the Origin:

“We thus see that the first stages of the transit of the eye from one side of the head to the other, which Mr. Mivart considers would be injurious may be attributed to the habit, no doubt beneficial to the individual and to the species, of endeavoring to look upwards with both eyes, whilst resting on one side at the bottom. We may also attribute to the inherited effects of use the fact of the mouth in several kinds of flat-fish being bent towards the lower surface… But it cannot be supposed that the peculiar speckled appearance of the upper side of the sole, so like the sandy bed of the sea, or the power in some species… of changing their colour in accordance with the surrounding surface, or the presence of bony tubercles on the upper side of the turbot, are due to the action of light. Here Natural selection has probably come into play, as well as in adapting the general shape of the body of these fishes, and many other peculiarities, to their habits of life. We should keep in mind, as I have before insisted, that the inherited effects of the increased use of parts, and perhaps of their disuse, will be strengthened by Natural selection…. How much to attribute in each particular case to the effects of use, and how much to Natural selection, it seems impossible to decide.”[19]

Modern evolutionary biologists do not accept any significant role for Lamarckian inheritance, leaving Darwin’s argument for selection as a plausible but still incomplete explanation: how exactly did the peculiar asymmetry of flatfishes evolve, and what were the potential functions of the first steps toward it? Only in the past couple of decades have new studies of fossils, evolutionary relationships, and larval development revealed what happened, when, and perhaps even why.

Recent studies of extraordinarily well-preserved fossils from the famous Monte Bolca locality in Italy, which date to the early Eocene epoch (ca 49 million years ago) have revealed intermediate stages between symmetrical and asymmetrical conditions[20]. These and other fossils, combined with a detailed analysis of evolutionary relationships based on data from living fishes, show that complete orbital migration arose in about 2.97 million years (although estimates of uncertainty indicate that it may have taken less than 470,000 years or as long as 7.96 million years)[21].

But exactly why and how did this bizarre shape change take place?[22] Studies of living flatfishes show that their larvae resemble typical bilaterally symmetrical fish that swim upright in the water column. Metamorphosis changes both their behavior and body shape, caused (as is also the case with metamorphosis in amphibians) by changes in thyroid hormone, but at different times. Behavior is first. One of the first changes in the larva is in the semicircular canals of the inner ear, which is accompanied by an increasingly tilted swimming posture. Only then do changes begin in the skull and eye position.

These observations support a hypothesis that the symmetrical ancestor of flatfishes may have been a mostly bottom-living fish with already established asymmetrical behavior (e.g., lying on one side and burrowing into the sand for ambush or shelter); eye migration and skull asymmetry may have evolved later to accommodate this change in behavior. Flatfishes can be either “dextral” (both eyes are located on the right side after metamorphosis) or “sinistral” (both eyes are located on the left side) morphology. The functional significance of the different arrangements is unknown, but most living species are all one or the other. Those Eocene fossils, however, reveal that in ancestral flatfish species right-eyed and left-eyed forms occurred in approximately equal frequency. This may indicate that eye-sidedness was random in ancestral flatfishes, until developmental-genetic systems evolved to control eye-sidedness for reasons that we still don’t understand.

So what started this process? When threatened, some modern non-flatfishes also lie flat on their sides on the seafloor and briefly bury themselves in the sand, only to leap up and snatch unsuspecting prey. This suggests that the flatfish’s ancestor might have been a symmetrical open water fish particularly good at this kind of behavior. That behavior might have set up selection pressures to make its body more suitable for it, and variants with less symmetrical eyes and skulls were favored. If the ecological niche of bottom-living predator was empty in the Eocene (as the fossil record suggests), then these evolutionary changes may have taken place rapidly.

In other words, modern discoveries in anatomy, biochemistry, genetics, developmental biology, and paleontology appear to support Darwin’s counter argument to Mivart’s objection about the “incipient stages of useful structures”: changes in environment or behavior can alter the functional significance of other characteristics of an organism, setting up new selection pressures that can lead to new – even extreme – body forms, sometimes much more quickly than we might expect.

Un Naturalista

During the Beagle voyage, Darwin spent a great deal of time on dry land, especially in South America. During one of these excursions in August, 1832, Darwin’s occupation as “un naturalista” was explained to a suspicious local military official as “a man that knows every thing.”[23] While the description apparently did little to calm the soldier’s concerns, it was not far off. Darwin succeeded in convincing the world that evolution was true for many reasons, but one of the most important was his encyclopedic interest in all areas of the natural world. He saw evidence for evolution by natural selection everywhere, not just in finches, but in fossil sloths, human cranial bones, tongues of moths, shapes of flowers, and behavior of lizards, and also in the colors of fishes, the patterns of their distribution, the shapes of their bodies, and the seeds in their stomachs. Darwin succeeded because he understood so much about the natural world, and saw that his theory explained so much about it.

Acknowledgments

Thanks to Frank Sulloway for discussion, Kiera Crowley for assistance with illustrations, Matt Friedman for sharing an illustration, and Willy Bemis for discussion, illustrations, and comments on an earlier draft.

Notes

[1] See Allmon (2022).

[2] This essay draws heavily from the wonderful book Darwin’s Fishes by Daniel Pauly (2004) which is highly recommended for further details on many of the topics discussed here.

[3] Pauly (2004, p. xvii).

[4] Darwin in Barlow (1958, p. 27), quoted in Pauly (2004, p. 7).

[5] Edinburgh notebook (1827-9); CUL-DAR118 http://darwin-online.org.uk/content/frameset?viewtype=text&itemID=CUL-DAR118.-&pageseq=1

[6] For more on Darwin’s Beagle collections, see Porter (1985) and Allmon (2016).

[7] Pauly (200, p. xix)

[8] Darwin (1839, p. 13).

[9] Darwin in Stauffer (1975, pp. 382, 520); Pauly (2004, pp. 4-5).

[10] Darwin (1859, p. 1).

[11] Pauly (2004, p. 70).

[12] Darwin (1859: p. 327).

[13] Darwin (1868, v. II, p. 222).

[14] Darwin in Stauffer (1975, p. 374-375).

[15] Aestivation is different from hibernation. The latter is associated with response to cold temperatures and the former is associated with dryness; the word “aestivate” refers to “summer sleep”.

[16] Stauffer (1975, p. 384); Pauly (2004, p. 131).

[17] Darwin (1859, p. 399); Pauly (2004, p. 131).

[18] Mivart (1871, p. 50).

[19] Darwin (1869, p. 186-188).

[20] Friedman (2008)

[21] Harrington et al. (2016).

[22] This discussion is based largely on Friedman (2008); Schreiber (2013); Jabr (2014); and Harrington et al. (2016).

[23] This famous description was given to the commandant of a fortress called Argentina by James Harris, an Englishman who lived in Patagonia and who had offered to be a guide for the Beagle crew in their exploration of the area (see van Helvert and van Wyhe, 2021, p. 279). It was recorded for posterity by the Beagle’s captain, Robert Fitzroy (1805-1865) in his own published account of the voyage (Fitzroy, 1839, p. 104).

References and Further Reading

Allmon, W.D., 2016, Darwin and palaeontology: A re-evaluation of his interpretation of the fossil record. Historical Biology, 28(5): 680-706.

Allmon, W.D., 2022, Darwin and insects. Blog post, 1/28/22 https://www.priweb.org/blog-post/darwin-and-insects

Barlow, N., ed., 1958, The autobiography of Charles Darwin 1809-1882. With the original omissions restored. Edited and with appendix and notes by his grand-daughter Nora Barlow. Collins, London, 249 p.

Darwin, C., 1839, Narrative of the surveying voyages of His Majesty's Ships Adventure and Beagle, between the years 1826 and 1836, describing their examination of the southern shores of South America, and the Beagle's circumnavigation of the globe. Vol. III. Journal and remarks. 1832-1836. Henry Colbourn, London, 619 p.

Darwin, C., 1859, On the origin of species. John Murray, London, 502 p.

Darwin, C., 1868, The variation of animals and plants under domestication. 2 vols. Murray, London, 411, 486 p.

Darwin, C., 1869, On the origin of species. 5th ed. John Murray, London, 581 p.

Darwin, C., 1871, The descent of man, and selection in relation to sex. 2 vols. John Murray, London, 424, 476 p.

FitzRoy, R., 1839, Narrative of the surveying voyages of His Majesty's Ships Adventure and Beagle between the years 1826 and 1836, describing their examination of the southern shores of South America, and the Beagle's circumnavigation of the globe. Vol. II. Proceedings of the second expedition, 1831-36, under the command of Captain Robert Fitz-Roy, R.N. Henry Colbourn, London, 698 p.

Friedman, M., 2008, The evolutionary origin of flatfish asymmetry. Nature, 454(7201): 209-212.

Harrington, R.C., R.C. Faircloth, R.I. Eytan, W.L. Smith, T.J. Near, M.E. Alfaro, and M. Friedman, 2016, Phylogenomic analysis of carangimorph fishes reveals flatfish asymmetry arose in a blink of the evolutionary eye. BMC Evolutionary Biology, 16(1): 1-14.

Jabr, F., 2014, The improbable—but true—evolutionary tale of flatfishes. https://www.pbs.org/wgbh/nova/article/flatfish-evolution/

Jenyns, L., 1841, The zoology of the voyage of H.M.S. Beagle, under the command of Captain FitzRoy, R.N., during the years 1832 to 1836. Edited and superintended by Charles Darwin. Part IV: Fish. London, Smith, Elder and Co., 172 p.

Mivart, St G. J., 1871, On the genesis of species. MacMillan, London, 314 p.

Pauly, D., 2004, Darwin’s fishes. An encyclopedia of ichthyology, ecology and evolution. Cambridge University Press, Cambridge, UK, 340 p.

Porter, D.M., 1985, The Beagle collector and his collections. In The Darwinian heritage. D. Kohn ed., Princeton University Press, Princeton, NJ, p. 973–1019.

Schreiber, A., 2013, Flatfish: An asymmetric perspective on metamorphosis. Current Topics in Developmental Biology, 103: 167-194.

Stauffer, R.C., ed., 1975, Charles Darwin's Natural Selection: Being the second part of his Big Species Book written from 1856 to 1858. Cambridge University Press, Cambridge, UK, 708 p.

van Helvert, P., and J. van Wyhe, 2021, Darwin. A companion. World Scientific, Hackensack, NJ and Singapore, 466 p.