The morphology of some organisms seems to have remained unchanged over a long evolutionary history, as if evolution has stagnated. Recent studies have shown that this phenomenon may come not only from stable selection that keeps the trait unchanged, but also from directed selection that drives changes in the trait but changes the direction frequently.
Written by | Zhengting Zou (Institute of Zoology, Chinese Academy of Sciences)
From microbes to behemoths, life on Earth is diverse. In the midst of this fascinating diversity, there is one question that has sparked long-standing concern in the evolutionary biology community. That is, if evolution has led to morphological changes and diversity in organisms, why do some organisms seem to have never undergone a morphological change even after hundreds of millions of years of evolution? In recent years, a number of studies have shown that morphological evolution can occur rapidly, even between generations. However, the evolution of some species seems to have "stagnated", "standing still". Today's coelacanths, for example, are almost indistinguishable from their fossilized ancestors hundreds of millions of years ago.
After years of debate, evolutionary biologists have often explained this paradox by using stable selection to maintain the same biological traits. Until recently, a study published in the Proceedings of the National Academy of Sciences proposed an alternative explanation. The study pointed out that those animals that seem to have the same morphology may actually be constantly undergoing trait changes in short-term directional selection. However, on longer time scales, directional selection frequently changes direction, so much so that these trait changes cancel each other out, resulting in apparent evolutionary "stagnation".
The origin of paradox
The morphological and functional characteristics of organisms are called "phenotypes". In the study of biological evolution, by observing the morphological characteristics of organisms in extant species and fossil records, we can describe the changes of phenotypes in the process of evolution, and try to explain the internal driving mechanisms of these phenotypic changes and diversification.
Specifically, evolutionary biologists are interested in the "tempo and mode" of phenotypic evolution. The law of the speed and slowness of phenotypic evolution, or "rhythm", gives us valuable insight into the mechanisms that drive evolution, and has been noted in Darwin's research and discourse as early as Darwin's research.
According to Darwin, biological evolution is primarily the process by which heritable variations in species phenotypes accumulate from generation to generation driven by natural selection. Therefore, phenotypic changes should be slow and continuous "gradients" in evolutionary history; Starting from a common ancestor, the process of 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 On the Origin of Species: "Species of different classes and genera do not change at the same rate or to the same extent. In the oldest strata of the third season, a few surviving shellfish can be found in many extinct types. …… Silurian sea bean sprouts are almost indistinguishable from living species of the genus; However, most of the other mollusks and all crustaceans of the Silurian have changed dramatically. (On the Origin of Species, Chapter 10, "On the Succession of Organisms in Earthly History") These phenomena show that there are differences in the rate of phenotypic evolution in different species.
Obviously, this discrepancy needs to be explained mechanically. The morphology of the present species is similar to that of the fossil record, which means that this clade of the evolutionary tree lacks phenotypic changes over a long period of time, the so-called "stasis". For example, coelacanths are more closely related to tetrapods than to "true fish" such as carp, and are the first group of flesh-finned fishes to diverge, with the vast majority of species extinct more than 60 million years ago; The living coelacanths, on the other hand, contain only two species, and their morphological structure is almost identical to that of their Cretaceous ancestors in the fossil record, making them truly "living fossils". So what are the mechanisms that lead to the observation of evolutionary stagnation in phenotypic evolution dominated by natural selection?
Western Indian Ocean speartail morphology
A complete fossil of a coelacanth
Darwin believed that slowly and continuously phenotypic changes driven by natural selection, coupled with "incompleteness of the geological record", could explain the rate differences in phenotypic evolution. From the thirties of the 20th century, the development of statistics and the rediscovery of Mendelian genetics gave birth to "neo-Darwinism" (also known as Modern Synthesis). R. Fisher A. Fisher), Sewall Wright, J. Haldane. Evolutionary biologists such as B. S. Haldane and Theodosius Dobzhansky provided quantitative support for Darwin's theory: they used probabilistic models based on genetic laws to describe how species phenotypes evolve through natural selection within populations.
In the neo-Darwinian framework, phenotypes can be quantified: the value of each phenotype (or a combination of several phenotypic values) corresponds to the value of an organism's ability to survive and leave fertile offspring, i.e., fitness. A well-suited phenotype is beneficial for organisms.
Phenotypes are subject to several different selection effects depending on the relevant environmental conditions: when linear directional selection occurs, changes in the value in one direction are beneficial for the survival and reproduction of the organism, for example, it is beneficial for the organism to become larger; The nonlinear selection effects include stablizing, which is the most beneficial value, and disruptive selection, which is more beneficial when the value becomes larger or smaller. In the process of reproduction of biological populations, different selection actions lead to changes in the distribution of this phenotype in the population.
It is conceivable that directional selection can shift the phenotypic distribution in a certain direction, and the accumulation of generations will change the phenotype of the whole species. Stable selection, on the other hand, causes the phenotype of the species to "stay put". Thus, neo-Darwinism argues that long-lasting stable selection could explain the evolutionary stagnesis we observe in the fossil record.
Different selection patterns and their effects on population phenotypes (Graph: Lupin)
In 1972, paleontologist Stephen Gould et al. proposed the "Punctuated Equilibria" theory to explain the phenotypic evolution rate difference and evolutionary hysteresis. The punctuated equilibrium theory holds that the phenotype of the same species is in evolutionary stagnation over a long period of time, only "interrupted" by speciation events. Paleontologist S. Stanley M. Stanley attributes evolutionary stagnant to the gene flow of different populations within a species—as long as there are no different species that exist in reproductive isolation from each other, these populations will have a phenotype that is difficult to change because of the gene flow between each population. Gould et al. proposed developmental limitations to explain evolutionary stagnation: the delicate and complex developmental procedures of multicellular organisms may limit the possibility of significant phenotypic changes in species undergoing natural selection, which may also lead to evolutionary stagnation.
Gradual evolution of phenotypes and punctuated equilibrium theory (Graphic: Lupin)
However, neo-Darwinists argue that punctuated equilibrium cannot challenge the role of natural selection in phenotypic evolution and evolutionary stagnosis. Brian Charlesworth and Montgomery Slatkin et al. (1982) argue that developmental limitations are difficult to fully explain evolutionary stagnation: domestic animals exhibit large differences in phenotype under artificial selection, such as large differences in body size and appearance between domestic dog strains; Among the wild species, there are also cases of birch moths adapting quickly to color changes within 50 years due to industrial pollution. At the same time, phenotypic differences are not always related to speciation events, for example, the number of species evolved by the small yarrow (minnow) group in North America was several times greater than the number of sunfish species in a similar evolutionary time, but the degree of phenotypic change between the two taxa was comparable and was not related to the number of speciation events. Therefore, it is not uncommon for phenotypic evolution to be "gradual". In conclusion, neo-Darwinists believe that the cause of evolutionary stagnation is likely to be primarily stable selection.
But the stable choice of this explanation also faces difficulties. Directional selection patterns that keep phenotypes in a dynamic state abound in living species, while stable selection patterns that maintain a "optimum" of phenotypes are rarely observed and do not appear to be sufficient to explain the evolutionary stareuse that is common 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 stable selection, stable selection may have little effect on the fitness of individuals in the population, because everyone is already "almost good enough", so stable selection may exist in nature, but it is difficult to measure and verify it from a technical point of view. The ubiquity of evolutionary stasis and the rarity of stable selection constitute the so-called "Paradox of Stasis" in the field of phenotypic evolution.
Reflecting on the "paradox of stasis", the question here is actually the relationship between "rhythm" and "pattern". Consider a fitness landscape model: imagine the X and Y axes on the topographic map 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 indicates the suitability of the organism for the corresponding phenotype. The adaptation of a population of organisms to the environment can be seen as a process of climbing upwards in this topographic map. When we look at a part of the topographic map, such as the combination of all phenotypes in a population, and find that there is a "peak" of fitness, then the phenotypes of the population should be selected stably and tend to be concentrated at the top of the mountain; When this local topography is a slope and the suitability increases in a certain direction, this corresponds to directional selection, and the population phenotype will deviate from the current distribution and change in that direction. Thus, when we observe a "pattern" of evolutionary stare, believing that the population has reached the top of the mountain of fitness, the phenotype is subject to stable selection to remain unchanged in each generation; But has the actual "rhythm" of phenotypic change slowed down?
Fitness topographic map of the relationship between local shape and selection effect (Drafting: Lupin)
It is not difficult to imagine that the phenotype may "hover" around a certain fixed value, with directional changes in different directions due to certain factors in each generation; But over a longer historical period, the amount of net change accumulated by the phenotype can still be so small that it looks like a stagnosis. In 2016, an analysis of the large fossil record showed that the phenotype of static and directional changes actually traveled the same length of change over the same length of time, but the direction of change in the former was indefinite, so the net change was much smaller than that of the latter. This also supports the fact that "rhythms" and "patterns" do not necessarily match the time scale of geological history, and that the static phenotype is still evolving at the same rate.
In this way, the evolutionary stagnation of the phenotype does not have to be explained by stable selection. So what is the driving force behind this frequent change in phenotype on smaller time scales? It is a natural assumption that each generation (or a shorter period of time over which multiple generations) is subjected to directional selection in different directions, and thus changes in phenotype – indeed, in nature, the environmental factors that affect the survival of organisms are certainly full of variables, and therefore the effects of natural selection exerted on phenotypes cannot be immutable.
In 2006, Jonathan Losos and others at Washington University in St. Louis published a study in the journal Science that looked at a species of eulizard found in the Bahamas. Often on the ground when there are no natural predators, researchers face new survival challenges when they introduce another large ground predator to the island. At first, individuals with long hind legs were more likely to escape predation on the ground, but as the population gradually migrated to trees, individuals with short hind legs had better ability to climb trees. Over a period of three field observations over a year, the researchers did find that natural selection for populations shifted from a preference for long legs to a preference for short legs.
In the short term, the change in the direction of directional selection seems to be real.
In 2023, Rossos et al. published a field study of four species of lyzard species with different habits, which directly explored the dynamics of phenotypes that underwent long-term evolutionary stagnation in a short period of time. The two-and-a-half-year study was divided into five periods, and 11 phenotypic data from different individuals were measured in each period, such as forefoot length, head length, and so on. The results of these five measurements show that there is a "summit" in the fitness topographic map of these phenotypes if only the first and last two time points are looked at, and the phenotype itself does not change much around this optimal value, as if it remained static under stable selection. However, for each individual time period, the fitness topographic map is a "slope" and the direction of inclination is different for each time period. For example, in some periods, long legs are good for survival, but in others, short legs are more competitive. The direction and intensity of the choice fluctuates, and there is no obvious pattern of variation.
This result means that for each species of lizard, the fitness topographic map actually changes over time, more like a "seascape" than a landscape – imagine the shape of a wave on the surface of the sea at one moment, and it will definitely change at the next moment. The lizard population is subjected to a certain degree of directional selection in a certain direction in each generation. The phenotype that is most beneficial for survival for one period may not be advantageous or even harmful for another period of time. Due to the constant change in direction, the fitness appears to have a cumulative optimal value on longer time scales, and the phenotype will also stay around the optimal value, exhibiting evolutionary staleness.
Therefore, this study shows that the directional selection of fluctuating can lead to the evolutionary stagnation of phenotypes.
A "seascape" that changes over time leads to directional choices that change direction, and can also lead to evolutionary stagnation (Graphic: Lupin)
The "basis of the static movement", a seemingly simple and stagnant phenotypic evolution model, is the result of a complex and dynamic process of natural selection. Evolutionary biology research, because of its concern with history, often has to extrapolate events that have occurred in the past hundreds of millions of years using the phenomena observed at this point in time, and assume that some factors remain constant on the time scale. The ultimate goal of natural science research is to use concise and unified laws and mechanisms to explain the operation and changes of the research object, but without sufficiently detailed and accurate experimental observations, it may be difficult for us to discover and verify the complex mechanism underlying the concise laws.
In fact, Darwin had already pointed out that "differences in the rate of phenotypic evolution in different species" were "dependent on a number of complex contingencies", including "the favourable nature of variation", "the strength of hybridization", "the rate of reproduction", "slowly changing environmental conditions", and so on. With the continuous accumulation of biological big data and the continuous improvement of research methods, the complex changes of phenotypic evolution patterns and related biological factors, such as natural selection, at different time scales will continue to be interesting directions for researchers.
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