The units of phylogenetic analysis
• Premise: units should be “natural” units.
= monophyletic: derived from single common ancestor.
– Individuals
– Populations
– Species: monophyletic collections of populations.
– Higher taxa: more inclusive monophyletic collections
of populations.
• Most common unit is species.
–C
Collection
ll ti off populations.
l ti
– Distinguished from other species by some kind of
criterion: morphological, genetic, ecological.
– Two aspects: (1) definition and (2) diagnosis.
Species and speciation
• Why important in phylogenetics?
– Evolutionary tree: branching points (nodes)
represent speciation events.
– Process models to understand phylogenetic
relationships invoke models of speciation.
– Models of speciation depend on concept of what
species are.
– Biologists disagree about what species are.
• Origin of species is fundamental issue in evolutionary
biology.
• Can’t be resolved without agreement about what a
species is.
• Two primary contexts: phylogenetics and evolutionary
genetics.
1
The so-called “species problem” has plagued
evolutionary biology since before Darwin’s
publication of the aptly titled Origin of Species.
Species
Many biologists think the problem is just a matter
of semantics; others complain that it will not be
solved until we have more empirical data. Yet,
we don’t seem to be able to escape discussing it
and teaching seminars about it.
– M. Pigliucci
BioEssays 25:596
Discussions of the nature of species seem to
arouse passion and self-righteousness not found
in most “scientific” debates. Each side tends to
caricature
i t
the
th logic
l i off its
it opponents,
t emphasizing
h i i
the obvious weaknesses and not mentioning the
strengths. Furthermore, some of the issues
appear to be philosophical, not scientific. … it is
hardly surprising that the response of many
evolutionary geneticists has been to ignore (if not
disparage) these discussions.
– R.G. Harrison
In: Endless Forms, 1998
2
The appropriately militant view that systematists
need to embrace is that the responsibility for
species concepts lies solely with systematists.
systematists If
we continue to bow to the study of process over
pattern, then our endeavors to elucidate pattern
become irrelevant.
– Q.D. Wheeler & K.C. Nixon
Cladistics 6:79
Species concepts
• Do species always exist in nature? If so, why?
• Do species sometimes exist in nature? If so, why?
question: are species
p
real or
• Fundamental q
nominal?
– Realist concept: nature is divided into discrete
species.
• Basis: folk taxonomy.
• Ecologists seldom disagree over how many species
exist at a given location.
location
– Nominalist concept: species are artificial divisions of
a natural continuum.
• Basis: evolutionary lineages.
3
Species concepts
• Before Darwin, species were uncontroversial:
– Typological (essentialist) view dates from Aristotle.
– Formalized by Carl Linnaeus
(S t
(Systema
Naturae,
N t
1735)
Mus Nat Hist
Oxford Univ
• Darwin first to propose natural mechanisms for
evolutionary transformations of species.
– Laid groundwork for scientific study of speciation.
• Ironically, Darwin was a nominalist:
… I look at the term species, as one arbitrarily
given for the sake of convenience to a set of
individuals closely resembling each other
other…. In
short, we shall have to treat species in the same
manner as those naturalists treat genera, who
admit that genera are merely artificial
combinations made for convenience. This may
not be a cheering prospect; but we shall at least
be freed from the vain search for the
undiscovered and undiscoverable essence of the
term species.
– Charles Darwin, 1859
The Origin of Species
4
Nominalism and realism
• Other nominalists:
–
–
–
–
–
J.B.S. Haldane (1956)
P Raven
P.
R
(1976)
B.D. Mishler and M.J. Donoghue (1982)
G. Nelson (1989)
J. Mallet (2001)
• Semi-realist view common among botanists:
– Some species are real.
real
– Other groups less distinctive due to extensive
hybridization or clonal reproduction.
Species concepts
• Most modern biologists treat species as a
fundamental natural unit.
– Identify research organisms at species level.
– Communicate by Linnaean binomial.
• But little consensus on what species are:
– How to define the species category.
– How to recognize and diagnose species.
• Irony: evolutionary biologists commonly use the
term “species”
“
i ” with
i h seamless
l
exchange
h
off id
ideas.
– Only when someone is questioned on what is
meant by “species” does conflict arise.
• E.g.: endangered species.
5
Species concepts
• In practice, most species are recognized phenetically.
– Recognized by consistent differences in easily
identifiable morphological characters (traits).
– Diagnosed
g
by
y “reliable” characters:
• Possessed by all (or almost all) individuals.
• Not possessed by members of other species.
– Difficult to find characters relevant to all life stages.
– No reason why reliable characters should exist.
Golden
Go
den eagle
eag e
Bald eagle
Haliaeetus leucocephalus
Aquila chrysaetos
The consensus view (more or less)
• Species are sets of populations of organisms.
• Species are held together (rendered cohesive) by sex
and genetic compatibility.
– Conspecific individuals can potentially interbreed
interbreed.
• Species are kept separate from other species to the
extent that they do not fuse.
– Reproductively isolated from one another.
– Under ‘normal’ conditions.
• Species are the largest units that participate in
evolutionaryy p
processes (g
(gene flow,, adaptation,
p
, etc.))
– Genes replicate, organisms copulate, populations
evolve, species speciate.
• All have common history + genetic cohesion.
– Higher ‘taxa’ are groups of related species (clades).
• Clades have common history, but no cohesion.
6
Species concepts
• Practical problems of species
recognition:
– If species evolve from common ancestor,
expectt awkward
k
d intermediate
i t
di t cases.
• Differ on average, but with much variation.
• Sufficiently different to be recognized?
– No reliable characters for some closely related
“species”.
• Geographic variation: good character in one location
may be poor in another.
• Distinction is statistical rather than discrete.
• E.g., “ring species”: continuum rather than discrete.
Species concepts
• Example of ring species:
Ensatina salamanders of the
Pacific coast.
coast
• Spread south from Oregon on
both sides of San Joaquin
Valley.
7
Species concepts
• Another example of a ring species: Greenish Warblers of
northern and central Asia.
– Originated in Himalayas, spread westward and eastward around
Tibetan Plateau.
– Morphology
M h l
and
d songs b
become more complex
l iin b
both
th di
directions.
ti
– Reproductively isolated in Siberia.
West Siberian
species
East Siberian
species
Species concepts
• Controversy arises from conflict between:
(1) Intuitive classification of organisms (“kinds”).
• Similar taxonomies produced by different cultures.
(2) Continuous and complex process of evolution
evolution.
• No definition can neatly classify populations at every stage
of development.
• Why should expect distinct “species” rather than
continuous intergradation of interbreeding organisms?
• What kinds of genetic differences distinguish species?
• Species concepts influenced byy “causes” of
divergence:
– Selection.
– Drift, inbreeding (neutral theory).
– Founder effect and chromosomal speciation.
8
Species concepts
• Currently many formal definitions of species:
Agamospecies concept
Internodal species concept
Biological species concept
Morphological species concept
Cladistic species concept
Non-dimensional
Non
dimensional species concept
Cohesion species concept
Phenetic species concept
Composite species concept
Diagnosable phylogenetic species conc
Ecological species concept
Monophyly phylogenetic species concep
Evolutionary significant unit
General phylogenetic species concept
Evolutionary species concept
Polythetic species concept
Genealogical concordance concepRecognition species concept
Genetic species concept
Reproductive competition concept
Genotypic cluster concept
Successional species concept
g
species
p
concept
p
Taxonomic species
p
concept
p
Hennigian
Mayden, 1997
9
Species concepts
• Some species concepts define species at the
present: a single point in time.
(1) Phenetic species concept: overall similarity.
(2) Biological
Bi l i l species
i concept: iinterbreeding.
b di
(3) Genetic species concept: genetic isolation.
(4) Recognition species concept: recognition of
conspecifics.
(5) Ecological species concept: selection maintains
variation in forms we recognize
g
as species.
p
• Some concepts aim to define which individuals are
members of a species across time.
(6) Phylogenetic and (7) evolutionary species concepts.
Species concepts
(1) Phenetic species concept:
– Based on idea that species concept shouldn’t be tied to
any particular evolutionary model.
– Informally: species is a set of organisms that:
• Resemble one another in terms of overall similarity.
• Are distinct from other species.
– Formally:
• Would specify some exact degree of phenetic similarity.
• Similarity is measured by a phenetic distance statistic.
• E.g.,
g , a species
p
is a set of organisms:
g
– not more than x phenetic distance units apart.
– Separated by a phenetic distance of at least y units from
the nearest distinct set.
10
Phenetic species concept
– In practice, phenetic concept uses as
many characters as possible.
• Recognizes phenetic clusters using
multivariate statistics.
statistics
• Species consist of smaller clusters
that match level of similarity typical of
what would have been called a
species before numerical techniques
became available.
p
recognized
g
on basis of suites
• Species
of characters.
• Diagnostic characters are proxies for
underlying multivariate descriptions.
Distance
0
Phenetic species concept
– Simple extension of way species are recognized in
practice.
• Nature contains groups of organisms that are similar
phenetically.
phenetically
• Our perceptual systems operate a “cluster” algorithm.
• Different observers tend to agree on pattern of
similarity in most cases.
– Extensible to higher taxa (genera, families, etc.).
– Modern form of typological species concept?
11
Phenetic species concept
– Criticisms:
• Lacks sound philosophical basis.
– Underlying theoretical concept corresponding to a phenetic
cluster?
l
?
– Forced to make subjective and arbitrary decisions.
• No unique measure of phenetic similarity or distance.
– Different criteria can divide organisms into different sets of
groups.
– No criterion on which to fall back in ambiguous cases.
• No reason to suppose that a “real”
real pattern of
morphological types exists in nature.
– No variants in a population are more ‘typical’ or ‘real’ than
others.
Species concepts
(2) Biological species concept (BSC): defines species
in terms of interbreeding.
– Mayr: Species are groups of interbreeding natural
populations that are reproductively isolated from other such
groups.
– Most widely accepted species concept.
• Predates Darwin: John Ray (17th century).
• Strongly advocated by founders of modern synthesis:
– Dobzhansky, Mayr, Huxley.
– Places
Pl
species
i within
ithi conceptual
t l scheme
h
off population
l ti
genetics.
• Gene pool: abstract conception of set of interbreeding
organisms, within which gene frequencies can change.
• Species are (possibly subdivided) gene pools.
12
Biological species concept
– BSC explains why members of species:
(1) resemble one another,
(2) differ from other species.
– Shared gene pool gives species its genetic and
phenetic identity.
• Genes of organisms constantly reshuffled within gene
pool.
• Family lineages (parent, offspring, etc.) blurred by
gene transfer.
– Cohesiveness: selection favors sets of genes that
interact well with other genes to produce adapted
organisms.
– Genes not (usually) shared with other species.
Biological species concept
– Taxonomists usually identify species by morphology,
not reproduction.
• Morphological characters shared between individuals
are indicators of interbreeding.
• Seek morphological criteria that mimic the interbreeding
principle.
– Individuals of a species not morphologically uniform:
• Polytypic.
• Different species have different degrees of
morphological variation.
13
Reproductive isolating mechanisms
– Emphasis on reproductive isolating mechanisms (RIMs):
• Any property of two species that prohibits or reduces the
frequency of hybridization.
• Selected for by heterozygote disadvantage.
• Actual cases typically involve mix of several factors.
– Often classified into premating and postmating:
(1) Premating or prezygotic mechanisms: prevent formation
of hybrid zygotes.
– Ecological / habitat isolation: occur in different habitats in
same g
general region
g
((sympatric
y p
but allotopic).
p )
– Seasonal / temporal: mating or flowering occurs at different
seasons.
– Sexual / ethological: mutual attraction between sexes of
different species is weak or absent.
Reproductive isolating mechanisms
(2) Postmating or zygotic isolating mechanisms: reduce
viability or fertility of hybrid zygotes.
– Hybrid
y
inviability:
y hybrid
y
zygotes
yg
have reduced viability
y or are
inviable.
– Hybrid sterility: F1 hybrids of one or both sexes fail to produce
functional gametes.
– Hybrid breakdown: F2 or backcross hybrids have reduced
viability or fertility.
14
Species concepts
(3) Genetic species concept:
– Baker & Bradley (2006): We define a genetic species
as a group of genetically compatible interbreeding
natural populations that is genetically isolated from
other such groups.
– Focus on genetic isolation rather than reproductive
isolation:
• Can often be established with genetic data.
• Removes burden of demonstrating reproductive
isolating mechanisms
mechanisms.
– Based on population-genetics theory:
• Bateson–Dobzhansky–Muller (BDM) model.
• Allows for understanding and prediction of genetic
diversity and speciation.
Species concepts
(4) Recognition species concept:
– H.E.H. Patterson: species defined as a set of
organisms with a common method of recognizing
mates.
t
• SMRS: specific mate recognition system.
– In practice, defines species similar or identical to
the biological species concept.
• Two versions of general “reproductive species
concept”: key concept is interbreeding.
– Isolating mechanisms: prevent interbreeding
between species.
– Recognition mechanisms: ensure interbreeding
within species.
15
Recognition species concept
– Defining species by shared mate recognition has
advantages:
• May represent more accurately what happens when
new species originates:
– Crucial event may be evolution of new SMRS.
– Evolution of new isolating mechanisms might not be
important; might be incidental by-products of
divergence.
– And disadvantages:
• SMRS
S
S can’t
ca t be obse
observed
ed in dead spec
specimens.
e s
• Interbreeding more difficult to observe, usually
inferred indirectly.
Species concepts
(5) Ecological species concept:
– A species is a set of organisms exploiting a single
niche.
• B
Become diff
differentt species
i when
h migrate
i t among
environmental resources that exist in discrete forms.
– Forms and behavior of organisms are adapted to
resources exploited and habitats occupied.
• Ecological niche: set of resources and habitats
exploited by members of a species.
–P
Populations
l ti
form
f
discrete
di
t phenetic
h
ti clusters
l t
produced
d
d
by ecological and evolutionary processes controlling
division of resources.
– Based on theory of evolutionary ecology.
16
Ecological species concept
– E.g.: parasites evolve appropriate adaptations to
penetrate different hosts.
– Concept supposes that ecological niches in nature
occupy discrete “zones”:
• Adaptive zone: abstract space, set by resources and
competitors in nature, within which a type of “body plan” is
adaptive.
• Concept originally invented by G.G. Simpson for larger
categories of species (e.g., Mammalia), based on
Wright’s
Wright
s adaptive landscape.
landscape
• Hybrids fall between zones and are maladaptive.
• Hierarchy of zones corresponding to successive
taxonomic levels.
Evolutionary and phylogenetic
species concepts
• Reproductive and ecological concepts aim to define
how and explain why individuals should be grouped into
species at one instant in time.
time
– “Horizontal” species concepts.
• Other concepts needed to include all members of
species throughout its existence.
– “Vertical” species concepts.
– Might or might not include horizontal concepts.
17
Cladistic and phylogenetic
species concepts
A
B
C
(6) Cladistic species concept:
– Hennig: Species is a set of organisms
in a lineage between two branch points.
(7) Evolutionary species concept:
– Simpson: Species is a lineage (an ancestraldescendant sequence of populations) evolving
separately from others and with its own unitary
evolutionary role and tendencies.
– Closest to the ecological concept, with added time
dimension.
Cladistic and phylogenetic
species concepts
• Both concepts based on information about:
– Occurrence in fossil record.
– Phylogenetic relationships
relationships.
Ancestral species
(though observed later in fossil record)
Same species (though
observed at different
times in fossil record)
Different species
(though possibly
identical in form)
18
Species concepts as models
• Different species concepts are different models:
– Species concepts are simplifications aimed at
understanding and prediction.
– Differ in assumptions about what’s
what s important/unimportant
and relevant/irrelevant.
– Neither wrong nor right, just more or less useful.
Characteristics
associated
with species
Categories of
species concepts
(Pigliucci, 2003)
Species concepts as models
• Species concept, as a model, should be useful for
some purpose.
– Different concepts serve different purposes.
• Possible goals: define species so as to –
–
–
–
–
–
–
Correspond to discrete groups that we see in nature.
Help to classify groups in a systematic manner.
Help to understand how groups arise in nature.
Represent evolutionary history of groups of organisms.
Apply to the largest possible number of organisms.
Etc.
• No species concept can accomplish all of these goals.
• Identify the nature of one’s “species problem”, then
choose concept best at solving that problem.
19
Species concepts as models
• In particular, no concept can serve needs of both
evolutionary geneticists and systematists.
– Systematists:
y
• Fixed character-state differences between species.
• Inferences about phylogenetic relationships among
predefined terminal taxa.
– Evolutionary geneticists:
• Variation with “species”.
• Patterns of reticulation (mating)
(mating).
• Processes by which one lineage splits into two.
The essence of the “species problem” is the fact
that, while many different authorities have very
p
are,, there is no
different ideas of what species
set of experiments or observations that can be
imagined that can resolve which of these views is
the right one. This being so, the “species
problem” is not a scientific problem at all, merely
one about choosing and consistently applying a
convention about how we use a word
word.
– J. Brookfield
Genet. Res. 79:107-108
20