Transcript Slide 1

Topic 16. Lecture 22. Species and Speciation
What is species?
Species is a key concept used to describe biodiversity. Indeed, Darwin's book was called
"The Origin of Species". So, what is species? So, far we treated this concept simplistically,
saying that a species is a set of similar individuals, and if all individuals within a set are
similar, tightly related, connected, and compatible to each other, and, at the same time,
dissimilar, only distantly related, disconnected, and incompatible to all other individuals, we
are dealing with a "good species". Obviously, common ancestry of different modern
"species" implies that there could be no good species if we take into account all organisms,
modern and ancient.
If we are willing to consider only modern organisms, sometimes we encounter reasonably
good species.
Still, it is obvious that gradual evolution is inconsistent with all species being good. It does
not make sense to ask when exactly independent evolution of two lineages makes them
different species. How many grains constitute a heap? (one of Zeno's paradoxes).
Exactly how many years, after the Isthmus
of Panama has been formed, did it take for
isolated populations to become different
species? - A stupid question.
Indeed, very often modern species are not "good", and do not have definite boundaries.
On the one hand , connected forms can be
incompatible. Two reproductively isolated
forms are connected by a continuous "bridge"
consisting of perfectly fit intermediate forms.
On the other hand, disconnected
forms can be compatible. Two
rhododendrons, Rhododendron
catawbiense (North America, left)
and R. fortunei (China, right)
produce fertile hybrids (center).
Even within an apparently uniform "species", careful analysis often reveals some degree of
incompatibility between individuals from different populations (outbreeding depression).
Indeed, compatibility is not an all-or-nothing trait.
For example, crosses between individuals from different populations of a copepod
Tigriopus californicus result in backcross and F2 hybrid breakdown for a variety of fitness
related measures. The magnitude of this breakdown increases with evolutionary divergence
between populations (J. of Evolutionary Biology 19, 2040, 2006).
So are different populations of T. californicus different species? We must avoid asking such
questions too seriously.
OK, so what is species? We can characterize diversity of life from many perspectives, and
ask whether organisms from some set:
1) compete and interbreed with each other
(if yes, they belong to the same
population)?
2) are all similar to each other and
different from other organisms (if yes, they
belong to the same "form of life")?
3) are more closely related to each other
than to any other organism (if yes, they
belong to the same clade)?
4) are connected to each other (if yes, they
belong to the same "cluster")
5) are compatible to each other (if yes,
they belong to the same species).
Aquilegia
formosa
A.
pubescens
I prefer to reserve the word species for consideration of compatibility and incompatibility
between organisms. Different "species concepts" simply try to capture different aspects of
biodiversity, and it is important to avoid terminological confusions.
Using word "species" for consideration of compatibility and incompatibility is known as
"biological species concept", which defines species as
"a set of actually and potentially interbreeding populations, reproductively isolated from
other such sets" - a common definition of BSC.
This definition makes sense, if we understand interbreeding as a test for compatibility
(testing compatibility of asexuals is difficult, although the concept can be applied to them,
too). Still, is not flexible enough to describe reality (also, I prefer to consider individuals, and
not populations):
1) What if we find only a mild degree of reproductive isolation (outbreeding depression)?
2) What to do if transitivity is violated? Indeed, in some cases A can interbreed with B, B can
interbreed with C, but A and C are incompatible.
Transitivity (A = B and B = C imply A = C), along with reflexivity (A = A) and symmetry (A = B
implies B = A) is necessary to have good, non-overlapping classes. Trouble is, Nature does
not always cooperate.
It is better to think in terms of conspecificity of pairs of organisms ("binary", instead of
"unary" definition of species):
two individuals belong to the same species to the extent to which they are compatible to
each other, in the sense that any organism with a "mixed" genome will be fit. Speciation is
evolutionary origin of individual that are incompatible to their ancestors.
Every two humans are 100% (or nearly so) the same species, and a human and an elephant
are 100% different species.
100,000 years of
independent evolution still the same species
100,000,000 years
of independent
evolution - a
different species
500,000 years of independent
evolution. We might eventually
know if a H. sapiens can have
healthy kids with a H.
neanderthalensis.
If we have a set of individuals such that every two ones from the set are fully compatible to
each other, and each one is incompatible to anybody else, we have a "good species".
However, good species appear to be more of an exception than the norm, and there is no
usually need to argue whether two individuals "really" belong to the same species, if they
are in a grey area. Occasionally, this issue becomes important legally, but not scientifically,
due to Endangered Species Act.
A proposal to list polar bears
as protected avoids the issue
of whether they are a species.
Phylogenetically, polar bears
are nested within brown
bears, and they are probably
compatible to each other, at
least intrinsically.
So the really interesting issue is the origin of incompatibility between lineages that evolved
from the common ancestor. Indeed, this may look like a paradox: how can natural selection
(survival of the fittest) lead to low fitness of hybrids? It is possible for two incompatible
species to evolve from the common ancestor without violating dictate of natural selection?
The answer to the second question is
certainly "yes": horse-donkey
divergence never involved a mule
phase!
Still, the origin of incompatibility, or
speciation, is a fascinating process,
and it is now relatively wellunderstood, at least at the population
level.
Darwin already realized that
incompatibility between different
species “is not a specially endowed
quality, but is incidental on other
acquired differences,” (Origin of
Species, p. 245) and is caused by a
hybrid's “organization having been
disturbed by two organizations
having been compounded into one”
(p. 266).
As long as most of the possible genotypes are unfit, incompatibility between two genetically
distant genotypes must be a common occurrence. Of course, incompatibility does not mean
that speciation was involved with any drops in fitness: in many dimensions, there are many
ways around regions of low fitness.
In genetical terms, such curved ridges of fit genotypes,
responsible for incompatibility between distant enough
genotypes, correspond to incompatibility epistasis. In the
simplest case, we are dealing with a pair of loci, in which
some combination of allele is incompatible. This situation
is known as Dobzhansky-Muller incompatibility.
Incompatibility epistasis:
alleles A and B are OK
separately, but bad together.
For example, w ab = wAb = waB
= 1 but wAB = 0.2.
Speciation occurs when different lineages acquire new alleles that work well separately
(natural selection takes care of this) but do not work together in the same genotype (natural
selection does not care about this). Consider two loci, A and B. Suppose that the initial
genotype was aabb (assuming diploidy), after which one lineage accepted a -> A
replacement and became AAbb, and the other accepted b -> B replacement and became
aaBB. If the simultaneous presence of alleles A and B in the same genotype reduces fitness,
the two alleles constitute a Dobzhansky-Muller (DM) incompatibility.
Like individual deleterious alleles, DM incompatibilities can be either lethal or mild. Thus,
speciation can involve just one or many incompatibilities.
Also, DM incompatibilities can be either dominant or recessive (or intermediate):
i) dominant incompatibility - one copy of A together with one copy of B is enough to
reduce fitness. If F1 hybrids AaBb are unfit, incompatibility is dominant.
ii) recessive incompatibility - one copy of a together with one copy of b is enough to
maintain high fitness, and only AABB genotype is unfit, so that fitness declines only
in F2 and in later hybrid generations (hybrid breakdown).
Many DM incompatibilities are at least partially recessive, leading to "Haldane's Rule:
"hybrid sterility or inviability tends to afflict the heterogametic sex more than the
homogametic sex". Let as compare two cases:
1) Both A and B are autosomal loci
2) A is sex-linked and B is autosomal
AAbb x aaBB
|
AaBb
fit, if incompatibility is recessive
AAbb x a-BB
|
AaBb A-Bb
daughters are fit, but sons are unfit
In mammals and flies, males are the XY (heterogametic) sex, but in birds and butterflies
females are heterogametic (ZW). In the first case, hybrid sons often have lower fitness than
hybrid daughters, and the pattern is opposite in the other cases (there are only very few
exceptions).
A sterile female butterfly hybrid
A DM incompatibility can be:
1) hard (internal): a hybrid genotype is unfit under any conditions.
2) soft (ecological): a hybrid genotype is unfit only under some conditions
Even intermediate phenotype of hybrids can lead to soft incompatibility, if the intermediate
conditions are absent or rare in nature. Of course, ecological incompatibilities are harder to
study - this must be done outdoors.
Aquilegia
formosa
A.
pubescens
Ecological incompatibilities are important in defining species. Indeed, it would be insane to
lump into the same species every two individuals that are genetically compatible. We treat
the two Rhododendrons (or any two forms adapted to substantially different environments)
as separate species because we assume that, due to differences in their adaptations, their
hybrids would not find a suitable niche in nature. Again, there are unavoidable grey areas,
where such decisions are purely arbitrary.
Until very recently, nothing was known about genes that form DM incompatibilities. This is
now changing.
So, far, just one pair of such genes ("A and B") has been identified, that causes lethality of
in F1 hybrid males in matings between Drosophila melanogaster and D. simulans (Science
314, 1292 - 1295, 2006; Current Biology 17, R125-R127, 2007). These genes are Hybrid male
rescue (Hmr), functionally diverged in D. melanogaster, and Lethal hybrid rescue (Lhr),
functionally diverged in D. simulans.
When D. melanogaster females (red) are crossed to D. simulans males (blue), only sterile
hybrid daughters are produced because hybrid sons die. Left bars, sex chromosomes; right
bars, second chromosome; small hooked bar, Y chromosome. Hmrmel is incompatible with
Lhrsim, causing lethality of hybrid males. Hybrid daughters are viable because they are
heterozygous Hmrmel/Hmrsim.
Both Hmr and Lhr encode DNA-binding proteins - so far, it is not known how they interact
physically. A mutation of D. melanogaster Hmr and a mutation of D. simulans Lhr can, even
separately, restore viability of hybrid males. These mutations are compatible alleles at the
otherwise incompatible loci.
Both Hmr and Lhr evolved under unusually strong positive selection. Thus, hybrid fitness
problems are incidental byproducts of adaptive divergence, just as Darwin imagined.
However, it seems that this divergence was driven not by different ecological adaptations
but by genetic conflicts, involving selfish transposons.
Phylogenetic tree of Hmr. The number
shown above each lineage is the ratio of
non-synonymous (Ka) and synonymous
(Ks) substitution rates (Mol. Biol. Evol. 25,
2421-2430, 2008).
For other pairs of loci harboring incompatible alleles, only one member has been identified
so far. Matings between the same pair of species, D. melanogaster and D. simulans, lead to
incompatible interactions of D. simulans alleles of two autosomal genes that encode
components of the nuclear pore complex, nucleoporin 96kDa and nucleoporin 160kDa
(nup96 and nup160), with D. melanogaster alleles of one or more X chromosome loci (so far
unidentified). Again, nup96 and nup160 evolved under strong positive selection (Science
323, 779 - 782, 2009).
The ratio of non-synonymous (Ka) and
synonymous (Ks) substitution rates in
the evolution of Drosophila nup96.
How much divergence ensure accumulation of at least on lethal - or enough mild DM
incompatibilities? Very roughly, two lineages become incompatible when their genetic
distance exceeds 1-5%. There is a strong correlation between incompatibility and
dissimilarity. Incompatibility appears, very roughly, when the genetic distance between two
genotypes exceeds 0.01 - 0.05.
Each point represents a pair of species of Drosophila.
Phil. Trans. Royal Soc. B 353, 287-305, 1989.
No wonder that genotypes that are very dissimilar are also incompatible. However, it seems
that incompatibility kicks surprisingly abruptly. Still, there is no fixed "threshold of
incompatibility", in terms of the genetic distance.
In mammal clades with more invasive
placentas, maximal genetic distances
between pairs of hybridizable mammal
species are larger.
Placental invasiveness is quantified in
terms of the number of maternal cell layers
separating fetal tissues from the maternal
circulatory system (Am. Nat. 168, 114-120,
2006).
Invasive - black;
noninvasive - white.
Box plot showing cytochrome b and
12S genetic distance between
hybridizable pairs of mammals with
less invasive versus more invasive
placentation. Horizontal bars show
mean values; boxes show 95%
confidence intervals; error bars show
1SD either side of the mean.
Speciation
Speciation, the origin of species, is, in a sense, origin of incompatibility
between organisms. There are several modes of speciation:
1) Phyletic - in the course of evolution of one lineage it changes so
profoundly that current organisms and their remote ancestors must
be attributed to different species (here Zeno's paradox is obvious).
Naturally, phyletic speciation is hard to study.
2) Allopatric - two lineages evolve independently, because their ranges
do not overlap, and eventually become different species.
Allopatric speciation is not a specific process, but just a by-product
of independent divergence.
3) Sympatric - a (sexual) population splits into two species without
geographic isolation.
Sympatric speciation is a complex and fascinating process.
Allopatric speciation. Two geographically isolated lineages independently
accumulates positive selection-driven allele replacements (selectively neutral
replacements can hardly play a substantial role in speciation). Because evolution
is primarily divergent, these two lineages will mostly accumulate different derived
alleles and, eventually, will become incompatible to each other. The exact moment
of speciation can be determined (more or less) if we are dealing with singleincompatibility speciation - but not if it takes many weak incompatibilities to
cause complete lethality and/or sterility of hybrids.
The key property of allopatric speciation is Orr's snowball effect: accumulation of
incompatibilities accelerates with time since geographic isolation.
A derived allele fixed after the n-th allele
replacement (counting replacements in
both lineages) can be incompatible with n-1
alleles, derived or ancestral, that are
simultaneously present in the other
lineage).
Allele A must be compatible with
everything.
Allele B can be incompatible with A.
Allele C can be incompatible with B and a.
In other words, the target for incompatibility increases during divergence of the two
lineages. Thus, the rate of acquiring incompatibilities also increases, and he probability of
not acquiring at least one incompatibility declines.
After the n-th allele replacement is accomplished, the total number of possible
incompatibilities between the two lineages is 1, 2, ..., n-1 = n(n-1)/2. Let us assume that a
new allele and an allele at another locus with which it never occurred within the same
genome are incompatible with probability p. Then, the probability that none of potentially
incompatible pairs of alleles are actually incompatible is (1-p)n(n-1)/2 (a pair is compatible with
probability 1-p and we assume that compatibilities of different pairs are independent). Thus,
the probability of single-incompatibility speciation after the n-th replacement is
Prob(speciation) = 1 - (1-p)n(n-1)/2 ~ 1-exp(n2p/2)
A physicist would say that allopatric speciation involves a phase transition - for
some time, its probability is rather low, after which it rapidly reaches 100%. More
realistic models assuming that speciation requires many incompatible
interactions lead to similar conclusions.
Allopatric speciation is a ubiquitous and unavoidable process, although the time
between geographic isolation and speciation varies substantially.
Sympatric speciation of asexuals. Without sex, speciation can occur in sympatry (without
spatial separation) in the same way as in allopatry, as long as ecological differentiation
leads to independent regulation of densities of different organisms maintains two
independently evolving sympartic lineages (such as L and S bacteria in Lenski's
experiments), after which the same theory applies.
Indeed, an advantageous mutation within an L individual may eventually displace all L
individuals - but NOT S individuals (and vice versa). Of course, to actually measure
incompatibility of asexuals is very difficult - sex is a great experimental tool for studying
speciation.
Sympatric speciation with sex. This is a very interesting process. How can incompatibilities
accumulate within a single population? The population must somehow split into two,
without any external barrier, despite interbreeding. This process can occur only under
strong selection and, thus, it happens fast, if at all.
Thus, it is difficult to observe sympatric
speciation directly. However, there several
cases when a pair of similar species is almost
certainly a product of relatively recent
sympatric speciation: the two reproductively
isolated sister species live together and there
was simply no place for them to go to
speciate allopatrically.
1) Two cichlids in Lake Apoyo (Nature 439, 719-723, 2006). Apoyo is a young and small
volcanic crater lake in Nicaragua. It was seeded only once by the ancestral high-bodied
benthic species Amphilophus citrinellus, the most common cichlid species in the area, and
a new elongated limnetic species (Amphilophus zaliosus) evolved in Lake Apoyo from this
ancestral species within less than ~10,000 yr. The two species in Lake Apoyo are
reproductively isolated and eco-morphologically distinct.
The Midas cichlid (A. citrinellus)
and the Arrow cichlid (A.
zaliosus) are morphologically
distinct and use different diets.
2) Two palms on Lord Howe island (Nature 441, 210-213, 2006). A large dated phylogenetic
tree shows that the two species of Howea, endemic to the remote Lord Howe Island, are
sister taxa and diverged from each other well after the island was formed 6.9 million years
ago. There is a substantial disjunction in flowering time that is correlated with soil
preference. Several loci are more divergent between the two species than expected under
neutrality, a finding consistent with models of sympatric speciation involving
disruptive/divergent selection.
a, Lord Howe Island. b, The thatch palm, Howea
forsteriana, is characterized by multiple spikes in
each inflorescence and has straight leaves with
drooping leaflets. c, The curly palm, H. belmoreana,
bears a single spike and has recurved leaves with
ascending leaflets.
The flowering times of the two species are
strongly displaced. H. belmoreana is shown in
grey, H. forsteriana in black, with male (solid line)
and female (dotted line) phases.
3) Two buntings in the Tristan da Cunha archipelago (Science 315, 1420-1423, 2007).
Nesospiza buntings underwent parallel speciation on two small islands in the Tristan da
Cunha archipelago in the South Atlantic Ocean. On each island, an abundant small-billed
dietary generalist and a scarce large-billed specialist evolved sympatrically. Their
morphological diversity closely matches the available spectrum of seed sizes, and genetic
evidence suggests that they evolved independently on each island. Speciation is complete
on the smaller island, where there is a single habitat with strongly bimodal seed size
abundance, but is incomplete on the larger island, where a greater diversity of habitats has
resulted in three lineages.
The Tristan da Cunha archipelago
includes Inaccessible Island (14
km2) and Nightingale Island (4
km2). An unrooted tree shows
clear genetic distinction between
island populations.
Nesospiza acunhae
Speciation is complete on the Nightingale
island, but not on the Inaccessible island. A
bimodal distribution, in fact, may be a stable
state of the population, without necessarily
progressing to speciation.
Variation in male Nesospiza bill and body size. (A) shows greater morphological segregation
on Nightingale Island (N. wilkinsi and N. questi) than on Inaccessible Island (all other taxa),
where hybridization occurs. Bill sizes match peaks in the abundance of seeds of different
sizes on Nightingale Island and in each of the three main habitats on Inaccessible Island (B).
Simpatric speciation is not limited to small lakes or islands, but it is easier to demonstrate
there. It is probably common in organisms that are ecological specialists, and rare or absent
in generalists. It is hard to imagine sympatric speciation in elephants.
Situations intermediate between allopatric and sympatric speciation are also possible, and
they are collectively called parapatric speciation. Parapatric speciation is formation of two
species out of a spatially structured population without complete geographic isolation.
So, how can sympatric speciation happen? First, selection is needed to tear the population
apart. Second, there must be a mechanism of non-random mating, to make different favored
genotypes reproductively isolated from each other. At least two modes of selection can lead
to sympatric speciation:
1) disruptive selection acting on 1 quantitative trait
2) incompatibility selection acting on 2 (or more) traits.
If there are two traits that determine fitness, the efficiencies of utilizing resources I and II,
and two traits that determine non-random mating, male display and female preference,
sympatric speciation involves interactions between four quantitative traits. Analysis of the
corresponding models show that sympatric speciation could happen, if the genetic load,
caused by selection against intermediates, is al least ~60% or higher.
Hybrid speciation (Nature 446, 279-283, 2007) is yet another possibility. Genetic evidence
suggests that it is common, even without polyploidy. Indeed, hybridization leads to a long
leap in the space of genotypes which can make new adaptive peaks accessible.
Adaptive landscape in the space of
possible genotypes or phenotypes.
Fitness optima are blue. Adaptive
landscapes are not rigid, but are
readily distorted by environmental
changes. Mean phenotypes of species
and their hybrids are shown as
crosses, and offspring distributions
as dots. Species 1 and 2 are adapted
to different optima. Selection acts
mainly within each species, so
hybrids are 'hopeful monsters', far
from optima (solid arrows). Hybrids
will often attain new optima if
unoccupied adaptive peaks are
abundant. Polyploid hybrids can have
a variety of advantages over their
parents. Homoploid hybrids have
fewer initial advantages, but their
progeny can have high genetic
variances via recombination. This
burst of variation can help them attain
new adaptive peaks (dotted arrow) far
from parental optima.
Hybrid zones are narrow regions where two rather different forms of life, inhabiting areas on
the opposite sides of the zone, meet and hybridize Hybrid zones are common, and can shed
light on the process of speciation. Hybrid zones can be classified in at least two ways:
1) According to history - a hybrid zone can be:
i) primary, if the two species which it separates were produced by parapatric speciation,
ii) secondary, if the hybrid zone is the result of a secondary contact.
2) According to the mechanism that maintains the hybrid zone:
i) gradient zones - two species separated by hybrid zone are adapted to
different environments,
ii) tension zones - the environments on the opposite side of the zone are rather
similar, but the two species are incompatible to each other.
Hybrid zones of all kinds have been described.
Aquilegia formosa
A. pubescens
A. formosa and A. pubescens form a secondary gradient hybrid zone in Sierra Nevada.
Hybrids do not show any signs of intrinsically reduced fitness.
Toads Bombina bombina and Bombina variegata form a hybrid zone that runs across
Europe. Adult toads show a preference for either ponds (B. bombina) or puddles (B.
variegata), but healthy hybrids are common within the narrow hybrid zone. Perhaps, this is
also a secondary gradient zone.
Bombina variegata
Bombina bombina
Map of the study area. Dark portions of the pie diagrams represent the mean frequency of B.
variegata alleles over all loci. The straight stippled line is our approximation of the center of
morphological hybrid zone in 1920s from old data (Evolution 60, 583-600, 2006).
A hybrid zone between A. majus pseudomajus and A. majus striatum. Analysis of 19 species
of Antirrhium with diverse floral phenotypes suggests that there is a U-shape ridge of high
fitness with-thin the 3-dimensional space of floral phenotypes. This cloud defines an
evolutionary path that allows flower color to evolve while circumventing less-adaptive
regions. Hybridization between two "subspecies" A. majus pseudomajus and A. majus
striatum, located in different arms of the U-shaped path yields low-fitness genotypes,
accounting for the observed steep clines at hybrid zones (Science 313, 963 - 966, 2006).
Flowers of 19 Antirrhinum
species used for studying
the space of flower
phenotypes.
Cloud obtained for flowers from 19
species represented in space of
flower phenotypes. Each point
shows the position of a single
flower. Examples of flowers from
different positions in the genotypic
space are illustrated.
Hybrids between A. majus
pseudomajus and A. majus
striatum, found in a narrow hybrid
zone on the border between France
and Spain, correspond to a fitness
valley, because the parental
"subspecies" are located in
different arms of the U-shaped
ridge of high fitness.
This may be a primary tension
hybrid zone.
Quiz:
Two lineages, I and II, diverged from their common ancestor, as shown below. Yes, all allele
replacements happened in one lineage - perhaps, it was adapting to a new environment. For
each new, derived allele list all alleles in the other lineage with which it could be
incompatible. If p is the probability that a new allele is incompatible with an allele of other
locus to which this new allele was never exposed, what is the probability that, at present,
lineages I and II are still compatible to each other (so that allopatirc speciation did not yet
happen)?