Some organisms have not changed in hundreds of millions of years. Has evolution really stagnated?

Some organisms seem to have remained unchanged in their morphology over a long period of evolutionary history, as if evolution has stagnated. Recent studies have shown that this phenomenon may result not only from stabilizing selection that maintains the trait unchanged, but also from directional selection that drives trait changes but in frequently changing directions.

Written by Zou Zhengting (Institute of Zoology, Chinese Academy of Sciences)

From microbes to giants, the earth's creatures are in all shapes and sizes. Amid this fascinating diversity, there is a question that has long attracted the attention of the evolutionary biology community. That is, if evolution leads to morphological changes in organisms and diversity, why do some organisms seem to have not changed their morphology at all even after hundreds of millions of years of evolution? In recent years, many studies have shown that morphological evolution can occur rapidly - even between generations. However, the evolution of some species seems to have "stagnated" and "stayed where it is." For example, today's coelacanths are almost indistinguishable from their fossil ancestors hundreds of millions of years ago.

After years of debate, evolutionary biologists have mostly used stable selection to maintain biological traits to explain this paradox. Until recently, a study published in the Proceedings of the National Academy of Sciences (PNAS) proposed another explanation. The study pointed out that animals that seem to have unchanged morphology may actually be constantly changing their traits in short-term directional selection; however, when observed over a longer time scale, directional selection frequently changes direction, so that these trait changes cancel each other out, resulting in the apparent evolutionary "stagnation."

The origin of the paradox

The morphological and functional characteristics of organisms are called "phenotypes". In the study of biological evolution, by observing the diverse morphological characteristics of organisms in existing species and fossil records, we can describe the changing patterns of phenotypes during evolution and try to explain the internal driving mechanisms of these phenotypic changes and diversifications.

Specifically, evolutionary biologists are interested in the "tempo and mode" of phenotypic evolution. The regularity of the speed of phenotypic evolution, or the "tempo", gives us valuable information about the driving mechanism of evolution, and has been paid attention to as early as Darwin's research and discussion.

According to Darwin, biological evolution is mainly a process in which heritable variations in species phenotypes accumulate from generation to generation under the drive of natural selection. Therefore, in the history of evolution, phenotypic changes should be slow and continuous "gradual changes"; starting from a common ancestor, the gradual differentiation of different species should produce some "intermediate types." However, the fossil record does not prove this inference.

Regarding the rate of phenotypic evolution of species, Darwin wrote in "The Origin of Species": "Species of different classes and genera have not changed at the same rate or to the same extent. In the oldest strata of the Tertiary Period, among many extinct types, a few living shellfish can still be found. ... The Silurian sea buds are almost indistinguishable from the living species of the genus; however, most other Silurian mollusks and all crustaceans have undergone tremendous changes." ("The Origin of Species", Chapter 10 "On the Succession of Organisms in Geological History") These phenomena indicate that there are differences in the rate of phenotypic evolution among different species.

This difference obviously requires a mechanistic explanation. The morphology of living species is almost the same as that of fossil records, which means that this lineage on the evolutionary tree lacks phenotypic changes for a long time, which is called "evolutionary stasis". For example, coelacanths are more closely related to tetrapods than to "real fish" such as carp. They are the earliest differentiated group among lobe-finned fish, and most of their species became extinct more than 60 million years ago. However, the living coelacanths only include two species, and their morphological structure is almost exactly the same as their Cretaceous ancestors in the fossil record, making them veritable "living fossils". So in the process of phenotypic evolution dominated by natural selection, what mechanism causes us to observe evolutionary stasis?

Western Indian Ocean lanceolatus

A complete coelacanth fossil

Darwin believed that the slow and continuous phenotypic changes driven by natural selection, coupled with the "incompleteness of the geological record", could explain the differences in the rates of phenotypic evolution. Since the 1930s, the development of statistics and the rediscovery of Mendelian genetics have given rise to "neo-Darwinism (also called Modern Synthesis)". Evolutionary biologists represented by RA Fisher, Sewall Wright, JBS Haldane, and Theodosius Dobzhansky provided quantitative support for Darwin's theory: they used a probabilistic model based on genetic laws to describe how species phenotypes evolve driven by natural selection within biological populations.

In the framework of neo-Darwinian theory, phenotypes can be quantified: each phenotypic value (or a combination of several phenotypic values) corresponds to the ability of an organism to survive and leave fertile offspring, that is, fitness. Phenotypic values ​​with high fitness are beneficial to organisms.

Phenotypes are subject to several different types of selection depending on the relevant environmental conditions: when linear directional selection occurs, a change in value in one direction is beneficial to the survival and reproduction of the organism, such as becoming larger; while nonlinear selection includes stablizing selection, where a value that is neither too large nor too small is most beneficial, and disruptive selection, where both increasing and decreasing values ​​are more beneficial [1] . During the reproduction of a generation in a biological population, different selection effects lead to changes in the distribution of the phenotype in the population.

As you can imagine, directional selection can cause the phenotypic distribution to shift in a certain direction, and the accumulation of generations will cause the phenotype of the entire species to change; while stabilizing selection will make the phenotype of the species "stay where it is." Therefore, neo-Darwinism believes that long-term stable selection can explain the evolutionary stagnation phenomenon we observe in the fossil record.

Different selection modes and their effects on population phenotypes (Graphic: Lupin)

In 1972, paleontologist Stephen Gould and others proposed the "Punctuated Equilibria" theory to explain the differences in phenotypic evolution rates and evolutionary stagnation. The Punctuated Equilibria theory holds that the phenotype of the same species is in evolutionary stagnation during a long period of evolution, and is only "interrupted" by speciation events. Paleontologist SM Stanley attributed evolutionary stagnation to the gene flow of different populations within a species - as long as different species with reproductive isolation are not formed, these populations will maintain the phenotype of each population near a certain "average value" due to the gene flow between each other, making it difficult to change. Gould and others proposed developmental constraints to explain evolutionary stagnation: the complexity of the developmental program of multicellular organisms may limit the possibility of species undergoing significant phenotypic changes during the natural selection process, which may also lead to evolutionary stagnation.

Gradual evolution of phenotypes and the theory of punctuated equilibrium (Graphic: Lupin)

However, neo-Darwinists believe that the theory of punctuated equilibrium cannot challenge the role of natural selection in phenotypic evolution and evolutionary stasis. In 1982, Brian Charlesworth, Montgomery Slatkin and others pointed out that developmental constraints can hardly fully explain evolutionary stasis: domestic animals show huge phenotypic differences under artificial selection conditions. For example, different breeds of domestic dogs have very different body shapes and appearances. Among wild species, there are also cases of rapid adaptation such as the birch moth changing color within 50 years due to industrial pollution. At the same time, phenotypic differences are not always related to speciation events. For example, in a similar evolutionary period, the number of species evolved from the minnow group in North America is several times the number of sunfish species. However, the degree of phenotypic variation of the two groups is similar, which has nothing to do with the number of speciation events. Therefore, "gradual" phenotypic evolution is not uncommon [2]. In short, neo-Darwinists believe that the cause of evolutionary stasis is likely to be mainly stabilizing selection.

However, the explanation of stabilizing selection also faces difficulties. In living species, directional selection patterns that keep phenotypes in dynamic change are common, while stabilizing selection patterns that keep phenotypes at an "optimal value" are rarely observed, which seems insufficient to explain the common evolutionary stagnation phenomenon in the fossil record. In this regard, some studies have pointed out that when a biological population has reached the "optimal value" and is in stabilizing selection, the effect of stabilizing selection on the fitness of individuals in the population may be small, because everyone is "almost good enough", so stabilizing selection may exist in nature, but it is difficult to measure and verify technically [3]. The prevalence of evolutionary stagnation and the rarity of stabilizing selection constitute the so-called "Paradox of Stasis" in the field of phenotypic evolution.

Recent studies suggest a new mechanism

Reflecting on the "stasis paradox", the problem here is actually the relationship between "rhythm" and "pattern". Consider a fitness landscape model: imagine the X and Y axes on the landscape as two dimensions of the number of phenotypes, forming a two-dimensional plane, that is, the phenotypic space; the Z-axis height of each point on the plane represents the fitness of the organism with the corresponding phenotype. The adaptation of biological populations to the environment can be seen as a process of climbing up in this landscape. When we examine a part of this landscape, such as the combination of all phenotypes in a population, we find that there is a "top of the mountain" of fitness, then the phenotype of the population should be subject to stable selection and tend to concentrate on the top of the mountain; and when this local terrain is a slope, the fitness continues to increase in a certain direction, which corresponds to directional selection, and the population phenotype will deviate from the current distribution and change in that direction. Therefore, when we observe the "pattern" of evolutionary stasis, we believe that the population has stood on the top of the fitness mountain, and the phenotype is subject to stable selection in each generation. However, has the actual "rhythm" of phenotypic change slowed down?

The relationship between the local shape of the fitness landscape and the effects of selection (Cartography: Lupin)

It is not difficult to imagine that the phenotype may "hover" around a fixed value, and in each generation it may change in different directions due to certain factors; however, over a long historical period, the net change in the phenotype can still be very small, which looks like stagnation. In 2016, an analysis of a large number of fossil records showed that in the same length of time, static phenotypes and directional phenotypes actually went through the same length of change, but the direction of change of the former was uncertain, so the net change was much smaller than the latter [4]. This also supports the fact that "rhythm" and "pattern" do not necessarily match on the time scale of geological history, and static phenotypes are still evolving at the same rate.

In this way, the evolutionary stagnation of phenotypes does not need to be explained by stabilizing selection. So what is the driving force behind the frequent changes in phenotypes on a smaller time scale? A natural assumption is that each generation of the population (or a shorter period of time lasting for multiple generations) is subject to directional selection in different directions, so the phenotype changes - indeed, in nature, the environmental factors that affect the survival of organisms are certainly full of variables, so the natural selection effect on the phenotype cannot be unchanging.

In 2006, Jonathan Losos and others from Washington University in St. Louis published a study in the journal Science[5], focusing on a species of anole lizard, Anolis sagrei, distributed in the Bahamas. A. sagrei often lives on the ground when it has no natural enemies. When researchers introduced another large ground predator, Leiocephalus carinatus, to the island, A. sagrei faced new survival challenges. At first, individuals with long hind legs were more likely to escape predation on the ground, but as the entire population gradually moved to trees, individuals with short hind legs had better tree climbing ability. In three field observations over a period of one year, the researchers did find that natural selection on the A. sagrei population had changed from preferring long legs to preferring short legs.

Changes in the direction of directional selection in the short term appear to be real.

In 2023, researchers such as Rossos published another field study on four species of anole lizards with different habits, directly exploring the dynamics of phenotypes that have undergone long-term evolutionary stasis in a short period of time [6]. The researchers divided the two-and-a-half-year study into five periods, and measured 11 phenotypic data of different individuals in each period, such as foreleg length, head length, etc. The results of these five measurements showed that if we only look at the beginning and the end of the two time points, there is a "peak" in the fitness topography of these phenotypes, and the phenotypes themselves do not change much near this optimal value, as if they remain stagnant under stable selection. However, for each individual time period, the fitness topography is a "slope", and the inclination direction is different in each time period. For example, in some time periods, long legs are beneficial to their survival, but in other time periods, short legs are more competitive. The direction and intensity of selection fluctuate, and there is no obvious pattern of change.

This result means that for each species of anole lizard, the fitness topography actually changes over time, more like a "seascape" than a landscape - imagine the shape of the waves on the sea at one moment, which will definitely change dramatically at the next moment. Anole lizard populations are subject to a certain degree of directional selection in a certain direction in each generation. The phenotype that is most beneficial to survival in a period of time may not have a survival advantage or even be harmful in another period of time. Because the direction is constantly changing, on a longer time scale, fitness seems to have a cumulative optimal value, and the phenotype will stay near the optimal value, showing evolutionary stagnation.

This study therefore suggests that fluctuating directional selection can lead to phenotypic evolutionary stasis.

The changing "seascape" over time leads to directional selection of changes in direction, which may also lead to evolutionary stagnation (Graphic: Lupin)

"Stillness is the basis of movement." The seemingly simple and stagnant phenotypic evolutionary pattern is actually the result of a complex and dynamic natural selection process. Since evolutionary biology studies are concerned with history, they often have to use the phenomena observed at this point in time to infer events that occurred hundreds of millions of years ago, and assume that some factors remain constant over time. The ultimate goal of natural science research is to use simple and unified laws and mechanisms to explain the operation and changes of the research object. However, without sufficiently detailed and precise experimental observations, we may find it difficult to discover and verify the complex mechanisms underlying the simple laws.

In fact, when referring to the “differences in the rates of phenotypic evolution in different species,” Darwin pointed out that this “depends on many complex contingencies,” including “the favorable nature of the variation,” “the strength of hybridization,” “the rate of reproduction,” “slowly changing environmental conditions,” etc. With the continuous accumulation of biological big data and the continuous advancement of research methods, the complex changes in phenotypic evolution patterns and related biological factors—such as natural selection—on different time scales will continue to be an interesting direction for researchers to pursue [7].

References

[1] Futuyma, DJ & Kirkpatrick, M. Evolution, xviii, 599 pages (Sinauer Associates, Inc., Publishers, Sunderland, Massachusetts, 2017).

[2] Charlesworth, B., Lande, R. & Slatkin, M. A Neo-Darwinian Commentary on Macroevolution. Evolution 36, 474-498 (1982).

[3] Haller, BC & Hendry, AP Solving the paradox of stasis: squashed stabilizing selection and the limits of detection. Evolution 68, 483-500 (2014).

[4] Voje, KL Tempo does not correlate with mode in the fossil record. Evolution 70, 2678-2689 (2016).

[5] Losos, JB, Schoener, TW, Langerhans, RB & Spiller, DA Rapid temporal reversal in predator-driven natural selection. Science 314, 1111 (2006).

[6] Stroud, JT, Moore, MP, Langerhans, RB & Losos, JB Fluctuating selection maintains distinct species phenotypes in an ecological community in the wild. Proc Natl Acad Sci USA 120, e2222071120 (2023).

[7] Rolland, J. et al. Conceptual and empirical bridges between micro- and macroevolution. Nat Ecol Evol 7, 1181-1193 (2023).

This article is supported by the Science Popularization China Starry Sky Project

Produced by: China Association for Science and Technology Department of Science Popularization

Producer: China Science and Technology Press Co., Ltd., Beijing Zhongke Xinghe Culture Media Co., Ltd.

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