Introduction

The term coevolution is used to describe cases where two (or more) species reciprocally affect each other’s evolution. So for example, an evolutionary change in the morphology of a plant, might affect the morphology of an herbivore that eats the plant, which in turn might affect the evolution of the plant, which might affect the evolution of the herbivore…and so on.

Coevolution is likely to happen when different species have close ecological interactions with one another. These ecological relationships include Predator/prey, parasite/host, species that compete with each other for resources, species in mutualistic relationships, and more.

Coevolution in mutualistic relationships

Many cases of coevolution can be found in mutualistic relationships. For example, plants and their pollinators are so reliant on one another and their relationships are sometimes so exclusive that biologists have good reason to think that “matches” between the two are the result of a coevolutionary process. Mutualism describes relationships in which each organism in the relationship benefits. For example, some plants have coevolved with their pollinators. The plants benefit from dispersal of their pollen or seeds and the pollinators benefit from a nutritional reward, often nectar. In this case, the appearance of the flower has evolved to attract specific pollinators and the pollinators have evolved to take advantage of the rewards offered by the plant and to effectively carry their pollen.

Some plants and pollinators fit each other so well that no one else will do. Yucca moths pollinate only yuccas. And any yucca plants grown outside their native habitat and away from the yucca moths must be pollinated by hand because no foreign pollinator has the right morphology to pollinate yucca flowers. Figs and fig wasps are even more specific. In fact, their coevolutionary history has bound them so tightly that they even speciate in sync with one another — there are now over 900 fig species, each pollinated by one specific wasp species!

Another example involves Central American Acacia species, which have hollow thorns and pores at the bases of their leaves that secrete nectar. These hollow thorns are the exclusive nest-site of some species of ant that drink the nectar. But the ants are not just taking advantage of the plant — they also defend their acacia plant against herbivores (Fig 10.2). This is an example of coevoluiton resulting from a mutualistic relationship where both the acacia and the ants benefit.

This system is probably the product of coevolution: the plants would not have evolved hollow thorns or nectar pores unless their evolution had been affected by the ants, and the ants would not have evolved herbivore defense behaviors unless their evolution had been affected by the plants.

Predator/Prey Coevolution results in a Coevolutionary Arms Race

Predator/prey coevolution can lead to an evolutionary arms race. Consider a system of plant-eating insects. Any plant that happens to evolve a chemical that is repellent or harmful to insects will be favored. But the spread of this allele will put pressure on the insect population — and any insect that happens to have the ability to overcome this defense will be favored. Thus, insects that are resistant to the plant’s defense will become more common in the insect population. This, in turn, puts pressure on the plant population, and any plant that evolves a stronger chemical defense will be favored and that stronger defense will become more common. This, in turn, puts more pressure on the insect population…and so on. The levels of defense and counter-defense will continue to escalate, without either side “winning.” Hence, it is called an arms race. This sort of evolutionary arms race is relatively common for many predator/prey systems.

Other predator/prey systems have also engaged in arms races. For example, many molluscs, such as Murex snails, have evolved thick shells and spines to avoid being eaten by animals such as crabs and fish. These predators have, in turn, evolved weapons, such as powerful claws and jaws, that compensate for the snails’ thick shells and spines (Figure 10.3).

A coevolutionary arms race: squirrels, birds, and the pinecones they love

In most of the Rocky Mountains, red squirrels are an important predator of lodgepole pine seeds (Fig 10.4). They harvest pinecones from the trees and store them through the winter. However, the pine trees are not defenseless: squirrels have a difficult time with wide pinecones that weigh a lot but have fewer seeds. Crossbill birds live in these places and also eat pine seeds, but the squirrels get to the seeds first, so those birds don’t get as many seeds.

However, in a few isolated places, there are no red squirrels, and crossbills are the most important seed predator for lodgepoles. Again, the trees are not defenseless: crossbills have more difficulty getting seeds from cones with large, thick scales. But the birds have a mode of counterattack: crossbills with deeper, shorter, less curved bills are better able to extract seeds from tough cones.

Close ecological relationships (like the consumer/prey relationship described above) set the stage for coevolution to occur. But did it actually happen in this case? To figure that out, we need evidence that suggests that the prey (the trees) have evolved in response to the consumer (squirrels or birds) and that the consumer has evolved in response to the prey. Researchers Craig Benkman, William Holimon, and Julie Smith set out to see if their observations would support the hypothesis of coevolution.

The scientists reasoned that if coevolution had occurred they would expect to observe the following:

Differences between pinecones from different regions: If the trees have evolved in response to their seed predators, we should observe geographic differences in pinecones: where squirrels are the main seed predator, trees would have evolved stronger defenses against squirrel predation, and where birds are the main seed predator, trees would have evolved stronger defenses against bird predation. This turned out to be true (Fig 10.5). Where there are squirrels, the pinecones are heavier with fewer seeds, but have thinner scales, like the pinecone on the left. Where there are only crossbills, pinecones are lighter with more seeds, but have thick scales.

Geographic differences between predators that correspond to differences in prey: If the crossbills have evolved in response to the pine trees, we should observe geographic differences in birds: where the pinecones have thick scales, birds would have evolved deeper, less curved bills, which are better for getting seeds out of tough cones, than they have where the pinecones have thin scales. This also turns out to be true (Fig 10.6).

So we have evidence that the trees have experienced natural selection and adapted to the birds (and the squirrels) and that the birds have adapted to the trees. (However, note that we don’t have evidence that the squirrels have adapted to the trees.) It’s easy to see why this is called a coevolutionary arms race: it seems possible for the evolutionary “one-upping” to go on and on…even thicker-scaled pinecones are favored by natural selection, which causes deeper-billed birds to be favored, which causes even thicker-scaled pinecones to be favored, and so on…

Endosymbiosis and the Evolution of Eukaryotes

The evolutionary origin of eukaryotes is tied to a remarkable coevolutionary relationship. All extant eukaryotes are likely the descendants of a chimera-like organism that was a composite of a host cell and the cell(s) of an alpha-proteobacterium that “took up residence” inside it. This major theme in the origin of eukaryotes is known as endosymbiosis, one cell engulfing another such that the engulfed cell survives and both cells benefit. Over many generations, a symbiotic relationship can result in two organisms that depend on each other so completely that neither could survive on its own. Endosymbiotic events likely contributed to the origin of the last common ancestor of today’s eukaryotes and to later diversification in certain lineages of eukaryotes (Figure 10.7). Similar endosymbiotic associations are not uncommon in living eukaryotes.

Prokaryotic Metabolism

Many important metabolic processes arose in prokaryotes; however, some of these processes, such as nitrogen fixation, are never found in eukaryotes. The process of aerobic respiration is found in all major lineages of eukaryotes, and it is localized in the mitochondria. Aerobic respiration is also found in many lineages of prokaryotes, but it is not present in all of them, and a great deal of evidence suggests that such anaerobic prokaryotes never carried out aerobic respiration nor did their ancestors.

While today’s atmosphere is about 20% molecular oxygen (O₂), geological evidence shows that it originally lacked O₂. Without oxygen, aerobic respiration would not be expected, and living things would have relied on anaerobic respiration or the process of fermentation instead. At some point between 3.2 and 3.5 billion years ago, some prokaryotes began using energy from sunlight to power anabolic processes that reduce carbon dioxide to form organic compounds (photosynthesis). Hydrogen, derived from various sources, was “captured” using light-powered reactions to reduce fixed carbon dioxide in the Calvin cycle. The group of Gram-negative bacteria that gave rise to cyanobacteria used water as the hydrogen source and released O₂ as a “waste” product about 2.2 billion years ago.

Eventually, the amount of oxygen resulting from photosynthesis built up in some environments to levels that posed a risk to living organisms, since it can damage many organic compounds. Various metabolic processes evolved that protected organisms from oxygen, one of which, aerobic respiration, also generated high levels of ATP. It became widely present among prokaryotes, including in a free-living group we now call alpha-proteobacteria. Organisms that did not acquire aerobic respiration had to remain in oxygen-free environments. Originally, oxygen-rich environments were likely localized around places where cyanobacteria were abundant and active, but by about 2 billion years ago, geological evidence shows that oxygen was building up to higher concentrations in the atmosphere. Oxygen levels similar to today’s levels only arose within the last 700 million years.

Endosymbiotic Theory

Endosymbiosis involves one cell engulfing another which, over time, results in a coevolved relationship in which neither cell could survive alone. As cell biology developed in the 20^th century, it became clear that mitochondria were the organelles responsible for producing ATP using aerobic respiration, in which oxygen was the final electron acceptor. In the 1960s, American biologist Lynn Margulis developed the endosymbiotic theory, which states that eukaryotes may have been a product of one cell engulfing another, one living within another, and coevolving over time until the separate cells were no longer recognizable as such and shared genetic control of a mutualistic metabolic pathway to produce ATP. In 1967, Margulis introduced new data to support her work on the theory and substantiated her findings through microbiological evidence. Although Margulis’s work initially was met with resistance, this basic component of this once-revolutionary hypothesis is now widely accepted, with work progressing on uncovering the steps involved in this evolutionary process and the key players involved.

Mitochondria and evidence supporting endosymbiotic theory

One of the major features distinguishing prokaryotes from eukaryotes is the presence of mitochondria in virtually all eukaryotic cells. Eukaryotic cells may contain anywhere from one to several thousand mitochondria, depending on the cell’s level of energy consumption, in humans being most abundant in the liver and skeletal muscles. Although they may have originated as free-living aerobic organisms, mitochondria can no longer survive and reproduce outside the cell.

Mitochondria have several features that suggest their relationship to alpha-proteobacteria and thus the endosymbiotic theory (Figure 10.7). Alpha-proteobacteria are a large group of bacteria that includes species symbiotic with plants, disease organisms that can infect humans via ticks, and many free-living species that use light for energy. Mitochondria have their own genomes, with a circular chromosome. Mitochondria also have special ribosomes and transfer RNAs that resemble these same components in prokaryotes. However, many of the genes for respiratory proteins are now relocated in the nucleus. When these genes are compared to those of other organisms, they appear to be of alpha-proteobacterial origin. In some eukaryotic groups, such genes are found in the mitochondria, whereas in other groups, they are found in the nucleus. This has been interpreted as evidence that over evolutionary time, genes have been transferred from the endosymbiont chromosome to those of the host genome. This apparent “loss” of genes by the endosymbiont is probably one explanation why mitochondria cannot live without a host.

Another line of evidence supporting the idea that mitochondria were derived by endosymbiosis comes from the structure of the mitochondrion itself. Most mitochondria are shaped like alpha-proteobacteria and are surrounded by two membranes; the inner membrane is bacterial in nature whereas the outer membrane is eukaryotic in nature. This is exactly what one would expect if one membrane-bound organism was engulfed into a vacuole by another membrane-bound organism. The outer mitochondrial membrane was derived by the enclosing vesicle, while the inner membrane was derived from the plasma membrane of the endosymbiont. The mitochondrial inner membrane is extensive and involves substantial infoldings called cristae that resemble the textured, outer surface of alpha-proteobacteria. The matrix and inner membrane are rich with the enzymes necessary for aerobic respiration.

The third line of evidence comes from the production of new mitochondria. Mitochondria divide independently by a process that resembles binary fission in prokaryotes. Mitochondria arise only from previous mitochondria; they are not formed from scratch (de novo) by the eukaryotic cell. Mitochondria may fuse together; and they may be moved around inside the cell by interactions with the cytoskeleton. They reproduce within their enclosing cell and are distributed with the cytoplasm when a cell divides or two cells fuse. Therefore, although these organelles are highly integrated into the eukaryotic cell, they still reproduce as if they were independent organisms within the cell. However, their reproduction is synchronized with the activity and division of the cell. These features all support the theory that mitochondria were once free-living prokaryotes.

Some living eukaryotes are anaerobic and cannot survive in the presence of too much oxygen. However, a few appear to lack organelles that could be recognized as mitochondria. In the 1970s and on into the early 1990s, many biologists suggested that some of these eukaryotes were descended from ancestors whose lineages had diverged from the lineage of mitochondrion-containing eukaryotes before endosymbiosis occurred. Later findings suggest that reduced organelles are found in most, if not all, anaerobic eukaryotes, and that virtually all eukaryotes appear to carry some genes in their nuclei that are of mitochondrial origin.

Plastids and evidence supporting endosymbiotic theory

Some groups of eukaryotes are photosynthetic. Their cells contain, in addition to the standard eukaryotic organelles, another kind of organelle called a plastid. When such cells are carrying out photosynthesis, their plastids are rich in the pigment chlorophyll a and a range of other pigments, called accessory pigments, which are involved in harvesting energy from light. Photosynthetic plastids are called chloroplasts (Figure 10.8).

Like mitochondria, plastids appear to have an endosymbiotic origin. This hypothesis was also proposed and championed with the first direct evidence by Lynn Margulis. We now know that plastids are derived from cyanobacteria that lived inside the cells of an ancestral, aerobic, heterotrophic eukaryote. This is called primary endosymbiosis, and plastids of primary origin are surrounded by two membranes. However, the best evidence is that the acquisition of cyanobacterial endosymbionts has happened twice in the history of eukaryotes. In one case, the common ancestor of the major lineage/supergroup Archaeplastida took on a cyanobacterial endosymbiont; in the other, the ancestor of the small amoeboid rhizarian taxon, Paulinella, took on a different cyanobacterial endosymbiont. Almost all photosynthetic eukaryotes are descended from the first event, and only a couple of species are derived from the other, which in evolutionary terms, appears to be more recent.

Cyanobacteria are a group of Gram-negative bacteria with all the conventional structures of the group. However, unlike most prokaryotes, they have extensive, internal membrane-bound sacs called thylakoids. Chlorophyll is a component of these membranes, as are many of the proteins of the light reactions of photosynthesis. Chloroplasts of primary endosymbiotic origin have thylakoids, a circular DNA chromosome, and ribosomes similar to those of cyanobacteria. As in mitochondria, each chloroplast is surrounded by two membranes. The outer membrane is thought to be derived from the enclosing vacuole of the host, and the inner membrane is thought to be derived from the plasma membrane of the cyanobacterial endosymbiont.

There is also, as with the case of mitochondria, strong evidence that many of the genes of the endosymbiont were transferred to the nucleus. Plastids, like mitochondria, cannot live independently outside the host. In addition, like mitochondria, plastids are derived from the division of other plastids and never built from scratch. Researchers have suggested that the endosymbiotic event that led to Archaeplastida occurred 1 to 1.5 billion years ago, at least 5 hundred million years after the fossil record suggests that eukaryotes were present.

Not all plastids in eukaryotes are derived directly from primary endosymbiosis. Some of the major groups of algae became photosynthetic by secondary endosymbiosis, that is, by taking in either green algae or red algae (both from Archaeplastida) as endosymbionts. Numerous microscopic and genetic studies have supported this conclusion. Secondary plastids are surrounded by three or more membranes, and some secondary plastids even have clear remnants of the nucleus (nucleomorphs) of endosymbiotic algae. There are even cases where tertiary or higher-order endosymbiotic events are the best explanations for the features of some eukaryotic plastids.

Acknowledgements and References

Adapted from UC Museum of Paleontology Understanding Evolution, www.understandingevolution.org. Retrieved from https://evolution.berkeley.edu/evolution-101/mechanisms-the-processes-of-evolution/coevolution/

Adapted from Clark, M.A., Douglas, M., and Choi, J. (2018). Biology 2e. OpenStax. Retrieved from https://openstax.org/books/biology-2e/pages/1-introduction