Evolution of Sex and Breeding Systems:
Compiled as a final-year zoology student at the University of Edinburgh, based on the information given in lectures.
Evolution of haploidy and diploidy
(Mable & Otto 1998, in BioEssays)
Advantages of haploidy - haploids are
smaller and have a larger relative surface area for absorbing nutrients so may
grow faster; haploids have a lower mutational load at equilibrium.
Advantages of diploidy - somatic
mutations are masked, DNA damage can be repaired using the homologous copy as a
template, diploid populations might evolve faster.
In haploids, mean fitness is
W=~1-µ (where µ is mutation rate), in diploids W=~1-2µ (double the mutational
load), assuming mutations are deleterious and have at least a small effect on
Adaptive mutations are fixed
more rapidly in diploid than in haploid yeast populations (Paquin & Adams
Haploid and diploid stages may coexist
because they exploit different niches (Hughes & Otto 1999).
Distinct mating types (e.g. in
yeast, Chlamydomonas) can evolve by
loss of one or other component of a cell surface recognition (Hoekstra 1982), and
help to avoid inbreeding.
Anisogamy (two sizes of gametes) can be
maintained if there is an accelerating relationship between gamete size and
fitness (k>1 where viability of gametes is proportional to (m1+m2)k and m is gamete size), and numbers of gametes
produced are inversely proportional to their size (Bell 1978).
Inbreeding vs. outbreeding
Selfing in hermaphrodites may
be prevented by spatial or temporal separation of male/female gamete release,
or by self-incompatibility (due to an S-locus with many different alleles).
Self-incompatibility in plants
may be sporophytic (incompatibility type of pollen controlled by S-locus of
plant that produces it), or gametophytic (incompatibility type controlled by
the haploid gene of pollen itself). It may be heteromorphic (heterostyly), in
which flowers of different incompatibility types are morphologically different.
Selfing rates can be estimated
from genotypes of parents and progeny (assuming selfing has no effect on
offspring survival and that pollinators are indiscriminate), or from
heterozygosity of population (assuming equilibrium).
Selfing rate, S = 2F / (1+F),
where F is 'fixation index', and 1 - F = observed heterozygote frequency / 2pq
Advantages of selfing -
reproductive assurance, saves resources, allows locally-adapted genotypes to
Selfish B-chromosomes are more
prevalent in outcrossing plant species - the fitness cost they impose upon the
host leads to them being purged from inbred lineages (Burt & Trivers 1998).
Outcrossing mechanisms are commoner
in long-lived species than annuals, due to annuals' need for reproductive
assurance (Barrett et al 1996). Distribution of selfing rates is highly
binomial, with extremes over-represented.
Cost of outcrossing - an
individual only transmits one copy of its genome to next generation, rather
than two. Selfing should thus be favoured if inbreeding depression is less than
0.5. A rare gene for selfing can spread rapidly, e.g. spread of homostyled
primroses in heterostyled populations (Crosby 1949).
Inbreeding depression is
lowered by the fact that inbreeding facilitates purging of recessive
Advantage of selfing is lowered
if it uses up pollen that could otherwise be exported (pollen discounting).
Why intermediate selfing rates
might persist: increasing disadvantage of selfing with successive generations
of inbreeding, local adaptation, inbreeding between relatives (which lowers
advantage of selfing relative to outcrossing), trade-offs
between male and female function (which cause fertility to be
Inbreeding depression of at
least 2/3 is necessary for initial spread of self-incompatibility genes. Once
self-incompatibility has arisen, rare S-alleles have an advantage, so large
numbers should evolve.
Selfing leads to increased homozygosity, and in the long term reduced diversity within
a population. In plants it leads to reduced investment in flower production,
high fruit/flower ratios, and increased allocation of resources to female
(Maynard Smith & Szathmáry 1995, in The major transitions in evolution)
An allele with 'meiotic drive'
is one that can increase its probability of being transmitted to the next
generation at meiosis. Such alleles are rare in nature because meiotic drive is
hard to achieve and there will be selection among the other genes in an
organism to resist it.
The segregation distorter (SD) gene in Drosophila produces a toxin inactivating any sperm with a
particular allele (Rsp+)
at a 'responder' locus. The two loci are tightly linked. A similar system (the
t-locus) occurs in mice.
B chromosomes are useless,
parasitic chromosomes, found in many groups, that
impose a fitness cost upon their host but persist because of their ability to
increase in number within a lineage (Burt & Trivers 1998). In some plant
tissues, B chromosomes multiply as a result of non-disjunction. In the
grasshopper Myrmeleotettix maculatus,
they move preferentially to the egg nucleus rather than the polar bodies.
Transposable elements of DNA
can replicate selfishly within a genome. Their spread is counteracted by
lowered fertility resulting from transposons' tendency to cause mutations or to
lead to the production of aneuploid gametes (as a result of 'ectopic
recombination' between elements at different chromosome locations).
Uniparental inheritance of
organelles may have evolved to avoid intragenomic conflict - it occurs even in
isogamous organisms (such as Chlamydomonas).
Selfish genetic elements may
distort the sex ratio. In the wasp Nasonia
vitripennis, maternal sex ratio (msr)
is a maternally-transmitted factor that causes females to produce mostly
daughters; son-killer (sk) is a
maternally transmitted bacterium that causes male eggs to die, and paternal sex
ratio (psr) is a B chromosome that
destroys other paternal chromosomes to produce a haploid male (males are better
than females at transmitting the B chromosome to their descendants). (Werren et
Sex determination systems
Sex determination may be
environmental (e.g. due to temperature in crocodilians) or genetic.
In male heterogamety, females are
XX and males XY; occurs in mammals, where maleness is due to Sry gene on Y chromosome (Graves 2002),
and in Drosophila, where ratio of X
chromosomes to autosomes determines sex.
In female heterogamety, males are
ZZ and females ZW; occurs in birds, Lepidoptera and various lower vertebrates.
In some species there is a
dominant gene M that causes development as a male regardless of karyotype, e.g.
in house fly Musca domestica
(reviewed by Shearman 2002).
In some lemmings, there is an
X* variant of X chromosome and X*Y individuals are female. In the wood lemming Myopus schistocolor, non-disjunction
means that X*Y females only produce X* eggs; in varying lemming Dicrostonyx torquatus there is no
non-disjunction and a quarter of zygotes are non-viable YY, but this isn't a
big problem because more embryos are implanted than survive to birth. In both
cases, X* has transmission advantage over X.
The fixation of such genes may
lead to the evolution of new sex chromosomes. There is evidence of transitions
between male and female heterogamety in evolutionary history.
Haplodiploidy (arrhenotoky), in
which unfertilised eggs develop as males, occurs in all Hymenoptera. Sex is
determined by a locus with multiple alleles at which heterozygotes are female,
and haploids (or homozygous diploids, though these are inviable or infertile)
are male. In some other groups (mites, scale insects, sciarid flies), all eggs
are fertilised but paternal genome is eliminated in males.
In some crustaceans (e.g.
maternally-transmitted endosymbionts such as Wolbachia override sex determination systems causing feminisation
of carriers (reviewed by Rigaud 1997).
When dioecy has evolved from
cosexuality, theory predicts a higher incidence of male heterogamety, which is
what is observed in plants (exception: strawberry), but this is not necessarily
expected when genetic sex determination has evolved from environmental sex
Environmental sex determination
will be favoured when relative fitness of sexes depends on environmental
conditions (e.g. in marine worm Bonellia
viridis, where larvae that settle next to females become male). A bias towards the sex with the lowest
average fitness across environments is expected (reviewed by Shine 1999).
Why should genetic sex
determination evolve? A gene conferring maleness will spread if sex ratio is
variable since it gains an advantage when males are rare; this creates a
male-biased sex ratio that favours evolution of 'female' genes too. Same
applies if a femaleness factor appears first.
Haplodiploidy may arise due to
a gene carried by the mother, to which haplodiploidy gives a transmission
advantage, provided the fitness of haploid males is at least half that of
Fisher (1930): equal resources
should be invested in male and female offspring,
because an investment ratio biased in favour of one sex would give a fitness
advantage to the other (it would be rarer and get more matings).
The hyperparasitoid wasp Encarsia tricolor, in which male eggs
are laid within female parasites, will lay 50:50 male/female eggs if eggs are
limiting, but if hosts are limiting, the ratio will depend on proportion of
already-parasitized hosts encountered (Hunter &
In polygynous species such as
red deer (Sheldon & West 2004), females in good condition should have more
sons since a male's fitness is more dependent on quality than female's fitness.
In blue tits, females with a more attractive mate lay more male eggs for
similar reasons (Sheldon et al 1999).
In parasitoid wasps, more
female eggs are laid in good (large) hosts since female quality is important
for fitness (fecundity depends on body size) but male quality is less important
(West & Sheldon 2002).
Sex-changing fish where big
males control harems will be female early in life and male later (Shapiro
Local Resource Enhancement - if one sex
of offspring stays behind as 'helpers' (e.g. male African wild dogs), more of
this sex should be produced. In Seychelles warblers, where helpers (female) are
only helpful in good territories, more female offspring are produced under
these conditions (Schwarz 1988).
Local Resource Competition (LRC) - where
one sex disperses, more of this sex should be produced since they are less
likely to compete with siblings. Suggested in primates, but evidence is not
clear (Brown & Silk 2002).
Most obvious example of LRC is
in social insects, where offspring of swarming species are strongly
Local Mate Competition is a specific
form of LRC. Female-biased sex ratios increase fitness of sons (more partners,
less competition between brothers) and increase relatedness of mothers to
daughters in haplodiploid species. Higher
inbreeding should lead to more female-biased sex ratios - observed in fig
wasps, where there is less inbreeding bigger figs containing more individuals
In Plasmodium and related apicomplexan parasites (where male
gametocytes can produce eight gametes but female gametocytes produce only one),
inbreeding favours female-biased sex ratios. Sex ratio is less biased where
transmission intensity (and thus number of clones per host) is higher (West et
Evolution of separate sexes
In both plants and animals,
dioecy evolved separately many, many times
Dioecy in plant lineages is
probably recent - this is inferred from its distribution and the fact that
unisexual plants often have opposite-sex rudiments. Dioecious lineages may have
short evolutionary lives.
Models for evolution
of dioecy assume trade-offs between male and female functions.
Advantages of dioecy vs.
hermaphroditism depend on gain curves - concave curves (intermediates have
higher fitness than pure males or females) favour hermaphroditism; convex
curves favour dioecy.
Evolution of two sexes requires
a minimum of two genetic changes, producing male sterility and female
Cytoplasmic male sterility
(e.g. in maize) will invade a population if it gives females even a slight
fertility advantage (leading to gynodioecy). Nuclear genomes may have genes
Nuclear male sterility genes
will invade if they double female fertility, or if
they help avoid inbreeding depression - both advantages are probably important.
Females producing 1+k times as many seeds as hermaphrodites
will be fitter if k > 1-2Sd where S is selfing rate and d is inbreeding depression.
Females are most likely to
invade hermaphrodite populations that allocate resources highly to male
Experiments on gynodioecious
populations fit the models well. In the gourd Cucurbita foetidissima there is intense inbreeding (Kohn 1988). In
New Zealand Umbelliferae, female frequencies increase with difference in
fertility between females and hermaphrodites (Webb 1979).
Female flowers may appear
hermaphroditic to fool pollen-seeking insects into visiting them (Charlesworth
Invasion of males into
hermaphrodite populations is not helped by inbreeding, since this simply
reduces availability of potential partners. Males can only invade if their
fitness is more than twice that of hermaphrodites. Androdioecy is therefore
rarer than gynodioecy. In the plant Datisca
glomerata, androdioecy has evolved from dioecy due to occasional need for
self-fertilisation (Fritsch & Rieseberg 1992). In Mercurialis annua, cosexuals devote a high proportion of resources
to female function and unisexual males have much higher pollen production
(Pannell 1997). In both species, denser populations (with higher outcrossing
rates) have a higher proportion of males.
In androdioecious nematode Caenorhabditis elegans, males persist
because they can mate with hermaphrodites but other hermaphrodites cannot.
In a newly-dioecious species,
linkage of male-sterility and female-sterility genes would be favoured to avoid
the production of sterile offspring carrying both. This may start the evolution
of sex chromosomes.
Why sex and recombination?
Types of sex: automixis
(selfing), amphimixis (outcrossing sex).
The union of haploid cells
(syngamy) can be explained by the advantage of masking different deleterious
alleles, but recombination requires a different explanation.
Recombination (mixing up of
genomes) occurs by crossing-over or by segregation of chromosomes.
Recombination in bacteria can
occur by transformation (uptake of DNA, which may be done primarily for
nutrition), transduction (transfer by a phage), or conjugation (transfer of
plasmids). It may be accidental. Bacterial sex may have evolved to benefit
selfish genetic elements by allowing them to spread (Maynard Smith &
Recombination in eukaryotes
probably evolved from DNA repair mechanisms; many enzymes involved have
homologues in prokaryotes (such as recA
in E. coli, which unwinds DNA so that
homologous strands can pair up). It
cannot simply be accidental side-effect of DNA repair, however - recombination
rates differ among organisms (male Drosophila
lack recombination, and artificial selection experiments can alter
recombination rates), and double-stranded DNA breaks are actually induced
Weissman argued that sex
evolved 'for the good of the species'. However, there must also be short-term
Selection among species does
help to maintain sex - asexual taxa go extinct rapidly (with some exceptions).
In insects, arrhenotoky
(unfertilised eggs becoming males) arose 8 times, including in some fairly
large taxonomic groups; thelytoky (unfertilised eggs becoming females) arose
~1000 times and is sporadically distributed.
In some groups parthenogenesis
occurs cyclically (e.g. aphids, gall wasps) or facultatively (e.g. nematodes,
The short-term advantage to sex
must be strong to overcome the disadvantages: meiosis is slow, courtship and
mating are costly, organisms risk not finding a mate, sexual selection may
lower survival, recombination breaks up favourable gene combinations (comparison
of chromosomes in male and female Drosophila
suggest that recombination reduces viability by ~1% and fecundity by ~7%).
In many cases selection has
reduced recombination rates: 'supergenes' (such as the clusters of genes that
determine appearance of mimics), Y chromosomes
The composition of the
population is only changed if there is non-random association between genes
Sibling competition may explain
the advantage of recombination and variety in some situations, although this
cannot be a general explanation. Experiments on Drosophila show that more variable families (those with different
fathers) compete less. Survivors of intra-family selection may compete better
with other families in later life.
Recombination may offer an
advantage in unpredictable environments. It will be favoured only if selection
favours positive associations of alleles in some generations and negative
associations in others (fluctuating epistasis).
adaptation, although only if there tend to be negative associations between
favourable alleles. Artificial selection experiments tend to raise
recombination rates (Otto & Lenormand).
Sex and recombination may help
maintain resistance against rapidly-evolving parasites (Hamilton 1980).
Many mutualists have lost the
ability to reproduce sexually (due to less need for rapid adaptation?).
Kondrashov suggested that
synergistic epistasis (the ability of organisms to tolerate moderate mutational
loads with little loss of fitness) could favour recombination, but this isn't
well supported by evidence, and would require an unrealistically-high mutation
Experiments with Chlamydomonas show that adaptation is
faster in bigger populations, but in asexual populations there are diminishing
returns with increasing population size, because in the absence of
recombination favourable mutations have to be acquired one after the other
Evolution of sex chromosomes
(Charlesworth 2002, in The Genetics and Biology of Sex Determination)
The X and Y chromosomes pair at
meiosis but fail to undergo recombination along some or part of their length.
Sex chromosomes evolved from
autosomes that acquired sex-determining genes. The mammalian X and Y have
ancient homologies (Lahn & Page 1999).
Sexually antagonistic genes -
those that favour one sex at the other's expense, such as guppy colour genes
(Fisher 1931) - become linked to the sex-determining locus, favouring
non-recombination between sex chromosomes.
In 'young' sex chromosomes,
non-recombination may be restricted to a small region, e.g. in papaya (Liu et
In bird sex chromosomes,
phylogenetic relationships between genes show that some sets stopped
recombining earlier than others (Lawson-Handley et al 2004).
Y chromosomes tend to accumulate
deleterious mutations because they never recombine, they exist at lower numbers
than other chromosomes in the population, and their genes are never homozygous.
Muller's ratchet is the
inexorable accumulation of deleterious mutations in the absence of
recombination, as the least mutation-loaded types are lost from the population
(Muller 1964). It is faster in smaller populations.
Background selection involves
the rapid loss of strongly-selected deleterious mutations from a
non-recombining population, carrying any new variants with them and decreasing
the effective population size.
When a highly beneficial allele
arises in a non-recombining population and goes to fixation (in a 'selective
sweep'), mildly deleterious mutations associated with it will also be fixed.
'Dosage compensation' ensures
that the activity of genes on the X chromosome is similar in males and females.
In Drosophila, X in males is
up-regulated; in C. elegans (where
hermaphrodites are XX and males X0), X is down-regulated in hermaphrodites; in
mammals, one X is inactivated in female cells. (Marín
et al 2000)
Many groups have 'neo-X' and
'neo-Y' chromosomes, with a pair of autosomes attached to the sex chromosomes.
In different Drosophila species, different stages of
degeneration of the neo-Y can be seen (there is no recombination in male Drosophila so the neo-Y totally stops
recombining). The neo-X shows signs of faster change in two adaptive genes (the
neo-X adapts faster than the neo-Y), the neo-Y shows faster change in other
genes (slightly deleterious mutations accumulate faster), and some neo-Y genes
have mutations that destroy their function. There is an excess of rare variants
of the neo-Y, perhaps due to 'selective sweeps'. (Bachtrog 2003/4)
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