Topic 16. Lecture 22. Species and Speciation

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.
2
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.
3
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).
4
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.
5
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).
A. pubescens
Aquilegia formosa
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.
6
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.
7
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.
500,000 years of independent evolution. We might
eventually know if a H. sapiens can have healthy
kids with a H. neanderthalensis.
100,000,000 years of independent evolution - a
different species
100,000 years of independent evolution - still
the same species
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".
8
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.
9
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
well-understood, 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).
10
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, wab
wAb waB 1 but wAB 0.2.
11
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 -gt A replacement and became AAbb, and
the other accepted b -gt 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).
12
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 x a-BB


AaBb

AaBb A-Bb fit, if incompatibility is
recessive 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
13
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.
A. pubescens
Aquilegia formosa
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.
14
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.
15
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).
16
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.
17
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.
18
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.
19
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.
20
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.
21
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 single-incompatibility 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.
22
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)
23
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. Allopat
ric speciation is a ubiquitous and unavoidable
process, although the time between geographic
isolation and speciation varies substantially.
24
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.
25
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.
26
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.
27
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.
28
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.
29
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.
30
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.
31
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.
32
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.
33
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.
34
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.
35
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).
36
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).
37
Flowers of 19 Antirrhinum species used for
studying the space of flower phenotypes.
38
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.
39
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)?