Thompson opens with "I explore what we have learned about why evolution is so relentless." While quite wordy, the book explores new aspects of evolution and provides numerous fascinating examples complete with refernces.
1 Adaptive Evolution
"If you read this book at the rate of about a chapter a day, by the time you finish it some [new microbial] species will have evolved."
A central argument is that evolution is as much an ecological process as it is a genetic process.
Examples of evolution that has occurred recently are sometimes called contemporary evolution, as seen in water fleas (Daphnia) and human influenza viruses.
Measurement of the rate of evolutionary change uses two units:
- the "darwin" - the change in value of a trait in natural logarithms per million years. Haldane: domesticated animals and plants “have changed in rates measured in kilodarwins.”
- the haldane - the change in standard deviations of a characteristic per generation, typically around 0.3
Overall, the longer the timescale over which the rate is estimated, the lower the estimate of the net rate of change. Longer timescales damp the shorter-term fluctuations.
"One of the important current challenges, then, in evolutionary biology is to understand how rapid evolutionary changes in life histories ripple throughout webs of interacting species, fostering yet more evolutionary change within and among ecosystems."
2 Natural Selection
The relatively simple act of harvesting wild populations for our own use has caused rapid evolutionary change in multiple species.
The evolution of pesticide resistance in agriculture has become common. It is problematical as imposing strong evolutionary change on any one of the pests has the potential to create a domino effect on the other species. Since the 1950s, Colorado potato beetles have evolved resistance to 52 different compounds, including all the major classes of insecticide.
In medicine, the resistance of bacteria to antibiotics is an ongoing concern. It has been shown that stopping the use of any given antibiotic does not necessarily result in the resistant forms being out-competed by the non-resistant forms. Resistance to chloroquine in Plasmodium falciparum, which is the most virulent malarial parasite, has evolved at least three times and spread among continents.
Directional selection causes a shift in the mean of traits. Stabilizing selection causes a decrease in the variance of a trait. Disruptive selection causes and increase in variance of a trait. The Lande-Arnold method allows selection on a trait to be partitioned into directional selection and nonlinear selection.
A current hypothesis is that selection is usually episodic, with occasional bouts of strong selection over timescales of decades.
3 Genes
Ronald Fisher argued that traits were determined by mutation and selection acting over many genes, each contributing in a small way. This is known as Fisher's infinitesimal model.
Sewall Wright argued that genes commonly affect multiple traits, and some genes mask the phenotypic effects of other genes. In his view, genes commonly affect multiple traits.
The new generation of genomic and bioinformatic techniques has provided further evidence that some traits are controlled by genes localized to one or a few positions on chromosomes, but other traits are controlled by genes distributed across the genome. Major genes, minor genes, and larger genomic processes are clearly all involved in adaptive evolution
On the other hand, flowering time in plants is controlled by the additive effect of many genes - for example, more than 60 in Arabidopsis. Human adult height is influenced by at least 180 loci.
Quantitative trait loci (QTLs) are regions of the genome that contain one or more loci contributing to phenotypic variation in a quantitative trait. Only two to six QTLs are needed to explain over 70 percent of the variation found in many dog morphological traits.
The odds ratio denotes the increase in risk of developing a disease - e.g. a ratio of 2 represents twice the risk. Most genes influencing human diseases have an odds ratio less than 2 and have an average near 1.3.
4 Genomes
Given a fitness landscape with adaptive peaks and valleys of gene combinations, evolution must move populations through a valley from one adaptive peak to another. Studies have shown that successful adaptation may often involve a moderate number of genes of varying effect rather than many genes of small effect
Whole genome duplication to form tetrapoids has been implicated in rapid evolutionary changes. Studies of Heuchera grossulariifolia in the Rocky Mountains show tetraploidy appearing three times with each form and the diploid differing in their insect herbivores and pollinators.
Hybridization is common in many taxa and contributes to rapid evolution. Surprisingly, although Swainson’s thrush migrate thousands of kilometers between their breeding sites and their overwintering sites, the populations remain separated during the breeding season.
5 Coevolving Genomes
Darwin pointed out that much selection has favored the manipulation of other species or defenses against other species. In the 1980s, the importance of parasites and symbiotic mutualists as major drivers of evolution started to become more evident
While the author states "We now know that symbiosis, living in intimate association in or on other species, is the most common lifestyle on earth", this refers to the broader picture of mutualism, parasitism and even services such as pollination.
Animals and plants have large assemblages of microbiota at various locations that evolve as an assembly and in conjunction with the host, an example being the gut bacteria which work with the immune system. In trees, the mycorrhizae provide minerals and water while defending against insect herbivores. The genes involved with immune function are generally the fastest evolving genes within vertebrates and invertebrates. The interaction between pea aphids and parasitoid wasps involves least six species: plant, aphid, two bacterial symbionts, bacteriophage, and parasitoid wasp. Most plants rely on six genomes: a nuclear genome, a mitochondrial genome, a chloroplast genome, mycorrhizal fungal genomes, a pollinator genome and a seed disperser genome.
6 Conflicting Genomes
The tension between conflict and cooperation ultimately affects the sizes of genomes. Parasites acquire genes that counter host defenses, while mutualistic symbionts often shed genes - often transferring some of their genes to their hosts. Viruses are in many ways the most successful lifestyle on earth - they have outsourced almost everything needed to sustain them, and in doing so they have become the most numerous form of life.
While about 0.36 percent of bacterial species are known to be pathogenic in humans, there is a curious lack of archaea that are known pathogens of eukaryotes. From the phage perspective, bacteria are simply vehicles that allow phages to infect eukaryotes. It is not known why phages have not coevolved with archaea to infect eukaryotes.
It is now known that microbial species can engage in social interactions mediated by chemical signals - quorum sensing. It is involved in the production of mucous to form the microbial mats called biofilms. Quorum sensing also has the potential to affect patterns of kin selection within microbial populations
7 Adaptive Variation
If most selection was directional, genetic variation within populations would be much more restricted than we observe. There is more variation in the individuals of a population than has been recognized. Examination of 179 humans from four populations revealed 15 million nucleotide locations that differed, most of this variation previously unknown.
The Grant and Grant studies of the Darwin "finches" (actually tanagers that have evolved finch characteristics) were important in showing that significant variation occurred over short time periods.
Two theories have been proposed to explain the maintenance of variation within populations. Heterozygote advantage proposes that individuals with two different allelic forms of a gene have higher Darwinian fitness in that environment than do individuals with only one form. Natural selection favoring relatively rare alleles results in frequency-dependent selection.
Populations retain a mix of defenses and counterdefenses that are favored or disfavored at different points in time.
Studies of the ecological drivers of fluctuating selection point to natural selection driven by parasites and pathogens as one of the major reasons why species continue to harbor so much genetic variation.
8 Recombination and Reproduction
The exchange of genes among individuals of a population, through sexual processes or other, leads to frequency-dependent selection that maintains variation in populations. There are two main theories as to how this occurs.
Muller's tachet posits that asexual clones tend to accumulate deleterious mutations over time, resulting in a ratchet-like decrease in fitness. The major alternative view is that sexual reproduction is common because it produces individuals with rare gene combinations that are more likely to escape from constantly evolving virulent parasites and pathogens.
Sexual reproduction is about being different rather than being better defended, which is an expanding theme in evolutionary biology
Horizontal gene transfer is pervasive in prokaryotes, highlighting the importance of gene exchange in the dynamics of evolution. Horizontal gene transfer between prokaryotes and eukaryotes appears to be relatively rare.
9 Divergence and Selection across Environments
Almost all species are groups of genetically distinct populations, and studies of protein variation have shown more variation than previously suspected. a species is often a large collection of semiindependent evolutionary experiments distributed across many environments.
Phylogenetic studies make it possible to track histories of species. Studies of Greya moths show how they have diversified over millions of years, initially feeding on Labrador tea, but groups forming that feed on saxifrages and on plants in the Carrot family.
While climate models have shown the ability to predict in which kinds of physical environment this species might be successful, other environmental factors are important including the presence of competitors, parasites, predators, and mutualists.
10 Local Adaptation
There are now hundreds of studies showing that individuals often survive, grow, or reproduce better in their normal environment than in other environments, thereby at least suggesting local adaptation driven by natural selection.
11 Coevolutionary Dynamics
The geographic mosaic theory of coevolution was developed as a framework for envisioning how coevolution proceeds among locally adapted populations living in contrasting environments. The outcome of the interaction between each pair of interacting genotypes may differ among environments.
Crossbills have bills specialized to extract seeds from different conifer species. Squirrels bite off scales to reach the seeds. The plants, in turn, show multiple adaptations to reduce successful attack by these seed predators. Where squirrels are abundant, they impose stronger selection on cones than do crossbills. Where squirrels are rare, conifers lack these defenses and often coevolve with crossbills. While this variation is found across North America, the presence or absence of squirrels does not confound coevolution with crossbills in the Caribbean.
12 The Geography of Traits and Outcomes
Prey / parasite populations should cycle between periods in which their traits are well matched and poorly matched as populations continue to coevolve. When traits are well matched between parasites and hosts, selection is especially strong on hosts; when traits are mismatched, selection is especially strong on parasites. In contrast, competition generally favors divergence of traits rather than matching of traits.
Once a species breaches the social structure of another species, it can follow multiple pathways of manipulating that species. An example is brood parasitism in birds, where traits can include eggs that mimic host eggs, tossing of host eggs out of the nest, killing of nest mates after hatching, and begging behaviors.
Invasive species provide opportunities for studying the pace and dynamics of the early stages of adaptive evolution. Parsnips, brought to North America in the 1600's, have escaped cultivation becoming a major weed in the midwestern United States. In the late 1800's, the parasitic parsnip webworm was found on parsnips. Now, various populations differ in their degree of matching and mismatching of chemical traits. Mismatching depends in part on the local presence of the native cow parsnip.
An example of evolution to changing environments is that of a popluation of blackcap warblers of western Europe which have recently changed their overwintering grounds from the Iberian peninsula to the United Kingdom. The birds migrating along the shorter northwestern migration route have rounder wings, narrower beaks, and some differences in plumage.
13 Experimental Evolution
Less than 8,000 prokaryotes (bacteria and archaea) and about 2,000 viruses have been formally described. However, it is expected that over a million species of each exist.
Work on the human microbiome has suggested that a human gut may harbor about 100 trillion microbial cells distributed over a thousand microbial species. Within each of us, evolution in those microbial communities is proceeding month after month and year after year.
Bacteria and viruses are not only by far the most common organisms on earth; they are also pitted against each other in never-ending battles.
Microcosm experiments, where a virus population is set against a bacterial population in a petri dish, provide a simple environment in which to study evolution. Bacteria only experiments have shown the evolution of new traits, such as the ability to metabolize citrates in E. coli, and the development of new forms in Pseudomonas.
Escherichia coli populations interacting with phages diverge into multiple resistant types within a few weeks - about 150 generations.
Microcosm studies suggest that coevolution accelerates evolution. Results also reinforce the developing view that antagonistic coevolution is often driven over the long term by forms of selection that maintain genetic variation in population rather than by sustained directional selection.
14 Ecological Speciation
Most current uses of the word species in evolutionary biology are based on the general view that species are groups of self-sustaining populations with traits, ecological attributes, and evolutionary trajectories that differ predictably from other groups.
Ecological speciation is the origin of reproductive isolation between populations driven by divergent natural selection on populations in different environments. Ecological speciation is therefore population divergence driven by poor adaptation of hybrids to either parental environment.
15 Reticulate Diversification
Hybridization is a source of new genetic material, but hydrids must compete against the parents that have adapted to the local conditions. The greater the range of environments in which two species co-occur, the greater the chance that hybrid species could form.
Hybrids may have a greater ability to compete with their parents in the early stages of adaptice radiation. The hybrid swarm hypothesis sees a greater abundance of hybrids increasing the range of relevant variation in these early stages. The Grants showed that hybrids of the Darwin finches have had the greatest effect during early stages of divergence.
Allopolyploids are formed through gene duplication. In plants, at least, they tend to develop new morphological traits and become new species. The Heucherina group within the Saxifragaceae, which includes Heuchera, Lithophragma and Mitella, shows great complexity due to hybridization and genome duplicationin spite of small radiation.
Some analyses suggest that speciation rates are often high during an initial explosive stage of divergence and then decline over time
16 Species Interactions and Adaptive Radiations
Yuccas have radiated into 34 recognized species, pollinated by yucca moths in the genus Tegeticula, which includes at least 20 species. It has been shown that the influence of the co-evolving yucca moths has been a stronger agent of selection than variations in the physical environment.
The idea of escape-and-radiate coevolution sees a temporal series of alternating starbursts of speciation on both sides of the interaction, forming entire clades with new defenses and counterdefenses. Studies of adaptive radiation suggest that divergence is often pulsed rather than smooth.
Cospeciation - as opposed to coevolution - is a macroevolutionary pattern of speciation in which two or more co-occurring lineages undergo matched speciation events during their phylogenetic history. An example is the evolution of insects with bacterial symbionts, such as Camponotus ants and their and their Candidatus bacteria.
17 The Web of Life
Complementarity of traits and convergence of species together generate a coevolutionary process that leads to formation of mutualistic webs, rather than pairs, of coevolving species. A minority of plant species have a pollination relationship with a single insect species; a small number of bird-pollinated plants have exclusive relationships with one bird species. Webs feature degrees of nestedness, asymmetry, and compartmentalization.
The lifestyles of generalist species such as honeybees and large tropical frugivores became possible only after webs have evolved into large sizes. These species rely on their ability to interact with a wide range of species within webs.
18 Our Changing Perceptions
Thompson addresses the question of whether evolution is prgressive, presenting the views of various academics, but noting that "... our general perception depends on our definitions."
"Discussions on the evolution of evolvability continue, but the interpretation is becoming increasingly complex."
19 Conclusions
The central conclusion from current work is that adaptive evolution is pervasive, relentless, and often surprisingly fast.