Evolutionary genetics of natural populations

Introduction

 Populations evolve through the actions of mutation, migration, selection and

chance.

 Genetic diversity arises from mutation, or is added by immigration, and is

removed by selection, or lost by sampling in small populations.

 The balance between mutation and selection results in a ‘load’ of rare

deleterious alleles.
 Factors controlling the evolution of populations

 Our objective in conservation genetics is to preserve species as dynamic entities,

capable of evolving to adapt with environmental changes.

 It is therefore essential to understand the natural forces determining

evolutionary change.

 This information is central to planning genetic management of threatened and

endangered populations.

 Since evolution, at its most basic level, is change in the genetic composition of a
population, it requires genetic diversity.
Factors controlling the evolution of populations

Consequently, we must appreciate how genetic diversity arises, what forms of

genetic diversity exist and how it is lost.

At its simplest level, evolution involves any change in the frequency of an allele
due to mutation, migration (gene flow), selection or chance. The roles of these
factors can be summarized as follows:

 mutation is the source of all genetic diversity, but is a weak evolutionary force
over the short term, as mutation rates are generally very low

 migration (gene flow) reduces differences among populations generated by

mutation, selection and chance
 Factors controlling the evolution of populations
 selection is the only force causing evolutionary changes that better adapt
populations to their environment

 chance effects in small populations lead to loss of genetic diversity

 fragmentation and reduced migration limiting gene flow generate random

differentiation among subpopulations derived from the same original source
population.

 An evolving population can be modelled as a complex system influenced by

mutation, migration, selection and chance, operating within the context of the
breeding system (Fig. 3.1).
Factors controlling the evolution of populations
 Factors controlling the evolution of populations

 To evaluate the importance of the components of an evolving population, we

model it with none of the factors operating, then with each of the factors
individually, followed by two at a time, etc.

 By so doing we can estimate the impact of each factor and what role it is likely to
play in evolution.

 Further, we can identify those circumstances where particular factors can be

ignored, as it is rare for all factors to have significant effects simultaneously.

 For example, mutations occur at very low rates, and we can often ignore them over
the short term.
 Origin and regeneration of genetic diversity
 Genetic diversity is the raw material upon which natural selection acts to bring
about adaptive evolutionary change.

 Most naturally outbreeding species with large populations carry a substantial

store of genetic diversity.

 Here we address the questions how is genetic diversity produced, and how quickly
is it regenerated if it is lost?
 Mutation

 A mutation is a sudden genetic change in an allele or chromosome. All

genetic diversity originates from mutation.

 The word mutation refers both to the process by which novel genetic
variants arise (through natural errors in DNA replication, mobile genetic
elements, chromosomal breakages, etc.) and to the products of the
mutational process (e.g. the white eye mutation in fruit flies).
 Mutation

In conservation genetics, we are concerned with:

 How rapidly does the process of mutation add genetic diversity to populations?

 How do mutations affect the adaptive potential and reproductive fitness of

populations?

 How important is the accumulation of deleterious mutations to fitness decline

in small populations?
 Mutation

 The most important mutations are those at loci affecting fitness traits, most
notably lethal or deleterious mutations.

 Some mutations such as the dark melanic allele in moths, actually increase
fitness in polluted areas, as moths carrying the mutation are better camouflaged
on blackened trees and so suffer less bird predation.

 However, many mutations that occur in non-coding regions of the genome and
those that do not result in amino acid substitutions in proteins (silent
substitutions) probably have little or no impact on fitness (neutral mutations).
 Mutation

 Neutral mutations are, however, important as molecular markers and clocks

that provide valuable information on genetic differences among individuals,
populations and species.

 The rate of mutation is critical to its role in evolution. Rates are low.

 For a range of loci in eukaryotic species, the typical spontaneous mutation

rate is one new mutation per locus per 100000 gametes (10−5) per
generation.

 Mutation rates are similar across all eukaryotes, apart from those for
microsatellites.
 Mutation
 Mutation rates per nucleotide base are clearly lower than for single loci as there
are typically 1000 or more bases per gene locus.

 Mitochondrial DNA has a much higher mutation rate than nuclear loci, making it a
valuable tool in studying short-term evolutionary processes.

 Mutation rates for quantitative characters are approximately 10−3 times the
environmental variance per generation for a range of characters across a range of
species.

 This apparently high rate, compared to single loci, is because a mutation at any of
the many loci underlying the character can affect the trait.
 Mutation

 Mutation is a recurrent process where new alleles continue to arise over time. It
is in fact a slow chemical reaction.

 We can model the impact of mutation on a population by considering a single

locus with two alleles A1 and A2 at frequencies of p and q, with mutations only
changing A1 into A2 at a rate of u per generation, as follows:
 Mutation
The frequency of the A1 allele in the next generation p1 is the frequency of alleles that
do not mutate, namely:

p1 = p0(1−u)

Thus, the frequency of the A1 allele declines. The change in frequency of the A1 allele
(∆ p) is the difference between the frequencies in the two generations:

∆ p = p1 − p0 = p0(1−u)− p0

∆ p =−up0
 Mutation
 Consequently, the frequency of A1 declines by an amount that depends on the
mutation rate u and the starting frequency p0. There is a corresponding increase
in the frequency of A2

 (∆ q =+up0).

 Since the mutation rate is approximately 10−5 for morphological mutations, the
maximum change in allele frequency is 10−5 when p = 1. This is very small and can
be ignored in many circumstances.

 When genetic diversity is lost from an entire species, it is only regenerated by

mutation. As mutation rates are low, regeneration times are very long, typically
taking thousands to millions of generations for single locus variation
 Migration and gene flow

 Unlike the slow process of mutation, mixture of alleles from two or more genetically
differentiated populations can rapidly restore genetic diversity.

 The benefits, and potential hazards, of managed gene mixing to restore genetic
diversity in endangered species .

 The gene pools of partially isolated populations diverge over time as a result of
chance and selection.

 Migration and subsequent interbreeding reduce such differences. The impact of

migration is illustrated by B blood group allele frequencies in human populations
across Eurasia.
 Migration and gene flow

 Prior to about 1500 years ago, the B allele was essentially absent from Western
Europe, but it existed in high frequencies in the east.

 However, between 1500 and 500 years ago, there was a succession of Mongol and
Tartar invasions of Europe. As was typical of such military invasions, they left a trail of
pillage and rape, and consequently left some eastern alleles behind.

 Note the gradual decrease in frequency of the B blood group allele from east to west
(termed a cline).

 The change in allele frequency due to migration is ∆ q =m(qm −qo)

 Migration and gene flow

 where m is the migration rate, qm the allele frequency in immigrants and qo the
frequency in the original population.

 Thus, the change in allele frequency from one generation to another depends on the
proportion of alleles contributed by immigrants, and on the difference in frequency
between the immigrants and the original population.

 Migration may have very large effects on allele frequencies and is much more
effective at restoring genetic diversity than mutation.
 Migration and gene flow

 For example, if immigrants are homozygous for an allele absent from the native
population, and 20% of the population in the next generation are immigrants,
then the immigrant allele increases in frequency from 0 to 0.2 in a single
generation.

 Many endangered species are threatened by gene flow (introgression) from

related non-endangered species.

 Equation 3.3 can be used to estimate the immigration rate from allele frequency
data. For example, approximately 22% of the genetic material in the Web Valley
population of endangered Ethiopian wolves derives from domestic dogs
(Example 3.1).
Migration and gene flow
 Selection and adaptation

 The physical and biotic environments of virtually all species are continually
changing. For long-term survival, species must adjust to these changes.

 Climates fluctuate over time, sea levels make and break connections
between landmasses, and ice caps advance and retreat.

 Pests, parasites and diseases evolve new strains, switch hosts and spread to
new locations, and new competitors may arise. Adaptive evolution has been
described in a large number of animals and plants.
 Selection and adaptation
 For example, evolutionary changes have been documented in animals for

 morphology,
 behaviour, colour form,
 host plant resistance,
 prey size, body size,
 alcohol tolerance,
 reproductive rate,
 survival, disease resistance,
 predator avoidance,
 tolerance to pollutants,
 biocide resistance, etc.
 Selection and adaptation
 Adaptive evolutionary changes to a wide range of conditions have been reported
in plants, including those to soil conditions, water stress, flooding, light regimes,
exposure to wind, grazing, air pollution and herbicides.

 Of particular concern during the ‘sixth extinction’ are the environmental changes
wrought by human activities.

 Global warming is occurring as a consequence of industrial and agricultural

practices. Species have to move, or adapt to these changed climatic conditions.

 Birds, butterflies and plants have already altered their ranges.

 Selection and adaptation
 Humans have also been responsible for translocations of species, extinction of food
species, and inadvertent or deliberate introduction of novel chemicals to the
environment.

 In many cases, adaptive evolutionary changes have been recorded in affected species.
Rabbits in Australia rapidly evolved resistance to the myxoma virus when it was
introduced as a control measure.

 Over 200 species of moths worldwide display melanism in polluted industrial areas.

 Several species of plants have evolved tolerance to heavy metals in the process of
colonizing polluted heavy-metal mine wastes and plants are progressively evolving
resistance to herbicides.
 Selection and adaptation

 Adaptation may take the form of either physiological or behavioural modifications

where individuals change to cope with altered conditions, or genetic adaptation
where natural selection alters the genetic composition of populations over several or
many generations.

 Physiological adaptations by individuals include modifications in haemoglobin levels

to cope with altitude, immune responses to fight diseases, induction of enzymes to
cope with altered diets, etc.

 Behavioural adaptations may include altered food preference, avoidance behaviours,

etc.
 Selection and adaptation
 There is however a limit to physiological adaptation. If environment changes are so
extreme that no individual can cope, then the species becomes locally or globally
extinct.

 Evolutionary change through natural selection is the long-term mechanism for coping
with environmental change. This is referred to as adaptive evolution.

 When adaptive evolutionary changes continue over time, they may allow a
population or species to thrive in conditions more extreme than any individual could
originally tolerate.
 Selection and adaptation
 Adaptive evolution is observed wherever large genetically variable populations are
subjected to altered biotic or physical environments.

 It is of major importance in five conservation contexts:

1. preservation of the ability of species to evolve

2. loss of adaptive evolutionary potential in small populations
3. most endangered species now exist only on the periphery of their historical range,
and must therefore adapt to what was previously a marginal environment
4. genetic adaptation to captivity and its deleterious effects on reintroduction success
adaptation of translocated populations to their new environment
 Selection and adaptation

 Selection arises because different genotypes have different rates survival and
reproduction, resulting in changes in the frequency of alleles.

 Alleles whose carriers produce relatively larger numbers of fertile offspring

surviving to reproductive age increase in frequency, while alleles whose
carriers have fewer offspring decrease in frequency.

 Selection operates at all stages of the life cycle. In animals this involves
mating ability and fertility of males and females, fertilization success of
sperm and eggs, number of offspring per female, survival of offspring to
reproductive age and longevity.
 Selection and adaptation
 In plants, selection can involve pollen production, ability of pollen to reach the
stigma of flowers, germinate, grow down the style and fertilize, number of ova,
viability of the fertilized zygotes, their ability to disperse, germinate and grow to
sexual maturity, and the fertility of the resulting plant.
 Recessive lethal
 To illustrate and model the action of natural selection we will examine an
extreme case, that of recessive lethals. These alleles do not impair the ability of
heterozygotes but all homozygotes die (lethal).

 For example, all individuals homozygous for chondrodystrophic dwarfism (dwdw)

in endangered California condors die around hatching time.

 The effect of selection against chondrodystrophy is modelled in Box 3.2. We begin

with a normal allele (+) at a frequency of p and the recessive lethal (dw) allele at
a frequency of q.

 With random mating, the genotype frequencies at zygote formation are the
Hardy--Weinberg equilibrium frequencies p2,2pq and q2.
 Recessive lethal
 However, the three genotypes have different survival. The important factor in the
genetic effects of selection is not the absolute survival, but the relative survival of
the three genotypes.

 For example, if the ++, +dw and dwdw genotypes have 75%, 75% and 0% survival,
the relative values 1, 1 and 0 determine the impact of selection.

 We term these values the relative fitnesses, where the genotype(s) with the
highest fitness are given the maximum value of 1.

 The frequency of surviving adults is obtained by multiplying the initial frequencies

by the relative fitnesses. For example, the frequency of lethal homozygotes goes
from q2 at fertilization to q2 × 0 = 0 in adults.
 Recessive lethal
 After selection, we have lost a proportion of the population (−q2), so the total no
longer adds to 1. We must therefore divide by the total (1 − q2) to obtain relative
frequencies, as shown.
Recessive lethal
 Recessive lethal
 Equation 3.5 demonstrates that the lethal dw allele always declines in frequency,
as the sign of  Δq is negative.

 Further, the rate of decline slows markedly at lower allele frequencies, as it is

dependent on q2.

 For example, if q is 0.5,  Δq is −0.167, while if q is 0.1,  Δq is −0.009. Example 3.2
uses equation 3.4 to calculate the change in frequency of the dw alleles in
California condors.

 Selection not only applies to lethals. Any allele that changes the relative fitness of
its carriers will be subject to selection. If the effect on fitness is small then the
change in allele frequency will be correspondingly smaller
Recessive lethal
 Genotype × environment interaction
 Differences in performance of genotypes in different environments are referred
to as genotype × environment interactions.

 They typically develop when populations adapt to particular environmental

conditions, and survive and reproduce better in their native conditions than in
other environment.

 Genotype × environment interactions may take the form of altered rankings of

performance in different environments or magnitudes of differences that vary in
diverse environments.

 A classical example is provided by the growth and survival of transplanted

individuals of the sticky cinquefoil plant from high, medium and low elevations in
California (Fig. 3.4).
 Genotype × environment interaction
 When grown in each of the three environments, strains generally grew best in
the environment from which they originated and poorest in the most dissimilar
environment.
Genotype × environment interaction
 Genotype × environment interaction

Genotype × environment interactions are of major significance to the genetic

management of endangered species because:

1. the reproductive fitness of translocated individuals cannot be predicted if

there are significant, but poorly understood, genotype × environment
interactions
2. success of reintroduced populations may be compromised by genetic
adaptation to captivity

3. superior genotypes under captive conditions may have low fitness when
released to the wild
 Genotype × environment interaction
4. mixing of genetic material from populations from different environments may
generate genotypes that do not perform well under some, or all, conditions
knowledge of genotype × environment interaction can strongly influence the
choice of populations for return to the wild