Download Species Concepts

August 21, 2009
Bioe 109
Summer 2009
Lecture 11
Part I: Species Concepts
- biologists today still have no clear idea of how many extant species exist.
- only about three million species in total have been described, and only about 1.5 million of
these in any great detail.
- estimates of the number of species actually present range from 5 million to over 100 million.
- why is there this great degree of uncertainty?
1. many species groups are very poorly studied.
- notably here are microorganisms and parasites.
- parasitologists estimate that perhaps between 30-40% of all species are parasitic.
- obviously, a great number of these are undescribed - they represent extrapolations from the
parasitic fauna known from well-studied groups like birds and mammals .
2. many environments are poorly sampled.
- tropical environments - both terrestrial and aquatic are poorly studied.
- the deep-sea is another.
3. as molecular approaches are applied to identifying species boundaries, more and more
“cryptic species” are observed.
- a cryptic species is indistinguishable from another species at the morphological level, but is
distinguishable at the genetic level.
- the existence of fixed genetic differences is de facto evidence that the two species do not
interbreed (if they did, the genetic differences would be eliminated).
- cryptic species are identified by genetic criteria, but are similar to the older term “sibling
species”.
Species concepts
1. The Typological Species Concept (TSC, Linnaeus).
- the typological species concept was developed by the systematists - most notably Linnaeus in
the mid 18th century
- a typological species may be defined as a group of individuals that differ from other groups
by possessing constant diagnostic characters.
- the typological species concept gets its name from the process, initiated by Linnaeus, of
collecting a representative, or “type” specimen for a given species, and preserving it in a museum
collection.
- this “type” specimen of the species was thus used as the yardstick for identifying diagnostic
characters of that species that differentiate it from other species.
- the typological species concept has three main difficulties:
1. polymorphism within populations
- conspicuous visible polymorphisms present problems.
2. variation among population
- it forces one to identify geographical populations that differ by one diagnostic character from
other populations as different species.
3. sibling or cryptic species
- these are species that are virtually indistinguishable in appearance but do not interbreed.
2. The Biological Species Concept (BSC, Dobzhansky, Mayr)
- this species concept had its origin with Darwin, but was not popularized until the modern
synthesis by Dobzhansky and Mayr.
- based on the observation that populations of different species often coexist with one another in
the same region, but do not interbreed.
Mayr (1940) defined the BSC as “species are groups of actually or potentially interbreeding
natural populations that are reproductively isolated from other such groups”.
Dobzhansky (1937): species are the largest and most inclusive reproductive community of
sexual and cross-fertilizing individuals that share a common gene pool.
- this is clearly the concept that Darwin believed (seen in his notebooks).
- a clear advantage of the BSC is that species status has little to do with the degree of phenotypic
difference exhibited between species.
- it also has a clear biological and genetic meaning.
- Mayr divided the BSC into the “nondimensional” and the “multidimensional” species
concept.
The nondimensional species concept:
- this concept can be applied only to species that are sympatric and synchronous (i.e., inhabiting
the same region at the same time).
- the nondimensional species concept is ideally suited to identifying sibling species that coexist
in the same area but do not interbreed.
- the disadvantages of this concept are that it does not allow us to deal with cases in which the
species are not sympatric or coincident in time.
- this is where the multidimensional species concept comes into play.
The multidimensional species concept:
- the multidimensional species concept deals explicitly with populations that are allopatric
and/or allochronic (i.e., inhabiting different regions and/or not overlapping in time).
- the important feature of this definition is whether or not the populations have the potential to
interbreed.
- if they do, then they are classified as the same species.
- if not, they are recognized as distinct species.
- the acid test remains, however, the capacity for interbreeding.
- the pooling of the non-dimensional and multi-dimensional species concepts results in the
biological species concept.
- the BSC represents the most influential and popular species concept in use today.
- it is not, however, universally accepted and suffers from a number of deficiencies.
Problems with the BSC
1. ,ot applicable to asexual species.
- this eliminates the BSC from being applicable to many organisms that reproduce asexually.
2. Hybridization commonly occurs in nature.
- the ability of different groups of organisms to interbreed varies considerably, and this
contributes further confusion to the question of biological species.
- many species of freshwater fishes, waterfowl, and terrestrial plants are capable of hybridizing
with other species.
3. Difficult to establish.
- for sympatric species, the BSC does not have a problem - the two species exist in the same
region but do not interbreed and thus are recognized as good biological species.
- for allopatric populations, there is a problem.
- the BSC classifies two geographical populations of organisms as a biological species because
they can potentially interbreed.
- this issue of the “potential” to interbreed is the problem, because we cannot carry out the
necessary crosses to establish this fact for many species.
- furthermore, just because we can successfully cross individuals (say in the laboratory, or in a
zoo) from two geographically distinct populations does not necessarily mean that such matings
would occur in nature.
3. The Evolutionary Species Concept (ESC, Simpson, 1951)
- this is a species definition developed by paleontologists who required a definition that would
allow them to identify fossil species.
- from Simpson, an evolutionary species is “a lineage evolving separately from others with its
own unitary evolutionary role and tendencies”.
Problems with the ESC
1. Is arbitrary.
- the ESC is compromised by how one measures “unitary evolutionary role and tendencies”.
- therefore, a species that changes slowly in morphology over a period of time may still constitute
an evolutionary species to one paleontologists, whereas another may decide that the form has
changed enough so that the species now should be recognized as something different.
2. Descriptive, not mechanistic.
- the ESC has nothing to say about the mechanisms by which species are maintained or by which
new species evolve.
4. The Phylogenetic Species Concept (PSC, Cracraft, 1983)
- unlike previous species concepts, the PSC is not concerned with the present properties of
organisms or their hypothetical future.
- instead, it attempts to define species on the basis of a common phylogenetic history.
- from Cracraft, the PSC is “the smallest diagnosable monophyletic group of populations
within which there is a parental pattern of ancestry and descent”.
- a monophyletic group is defined as being derived from a common ancestor and includes all
descendants of that ancestor.
- advocates of the PSC use molecular phylogenies to identify distinct monophyletic groups.
- one main advantage of the PSC is that it applies to all kinds of organisms - both sexual and
asexual.
Problems with the PSC:
1. What characters to use?
- should one identify species on the basis of neutral mutations?
- should genes reflecting the action of selection be given greater weight?
2. What level of divergence constitutes a species?
3. How do you distinguish between gene trees and species trees?
- phylogenies based on different genes may give different trees.
- the trick is to identify the tree that actually represents the true history of the species.
4. Does not address mechanism.
Part II: Speciation
- speciation is the process by which new species are formed from previously existing ones.
- in Darwin’s words speciation is the “multiplication of species”.
- species can thus be viewed to “reproduce” much like individual organisms.
- in fact, it is common to talk of a “parental” species giving rise to a “daughter” species (species
are like ships in that we don’t talk about “sons” being produced).
- although it is possible for us to draw a parallel between reproduction at the individual level and
reproduction at the species level, there is an important difference between these processes.
- individual organisms have been “programmed” by their genetic systems to reproduce.
- there is no such selection acting at the species level.
- if we use the biological species concept, speciation occurs when populations acquire
reproductive isolating mechanisms.
- these barriers may act to prevent fertilization – this is called prezygotic isolation.
- this typically involves changes in location or timing of breeding, or courtship displays.
- barriers may also occur if hybrids are inviable or sterile – this is postzygotic isolation.
- postzygotic barriers act after mating to prevent hybrids from backcrossing into either parental
species.
Modes of Speciation
1. Allopatric speciation
- most widely accepted mode of speciation.
- has wide support from studies on geographic variation among species.
- championed by Ernst Mayr, although the allopatric model of speciation is clearly the one that
was favored by Darwin as well.
- the first step in the process is the geographic separation of two populations of the same species.
- the isolation of the two populations has an immediate and important consequence:
it eliminates the movement of genes between the two populations.
- no gene flow allows the two populations to begin to evolve independently of one another.
- under the classic allopatric model the barrier that once separated the two populations is
eventually removed and the populations establish what is called “secondary contact”.
- what happens next is discussed in a later section.
2. Parapatric speciation
- parapatric speciation is similar to allopatric speciation but the two populations do not become
completely separated but remain connected over a narrow contact zone.
- the two populations begin to diverge genetically while continuing to exchange migrants across a
small zone of contact.
- commonly a hybrid zone is established.
- the width of the hybrid zone depends on the mean dispersal distance of the species involved and
the strength of selection.
- to produce a new species under the parapatric model, the strength of selection acting in the two
environments must be strong and the dispersal capabilities generally limited.
- in this regard, the parapatric model differs from the allopatric model.
- what is the evidence for parapatric speciation?
- evidence for parapatric speciation comes mainly from the existence of ring species.
- a ring species is a connected ring of species.
- for adjacent species that contact one another in their range, hybridization occurs.
- for species situated further apart in the ring, the ability to interbreed is diminished.
- for species located at the ends of these interconnected populations, reproductive isolation is
complete.
- a particularly interesting example of ring species in California involves salamanders of the
genus Ensatina.
- species of Ensatina diverge from the northern part of California and fold around either side of
the central valley.
- interbreeding occurs between species that make contact with each other on both sides of the
valley.
- when the two terminal species make contact at the southern end of the central valley, no
interbreeding occurs - isolation is complete.
3. Sympatric speciation
- sympatric speciation occurs when reproductive isolation is formed between two groups of a
population while they remain sympatric.
- recall that under the allopatric model the genetic divergence that occurs over time between the
geographically isolated populations is slow and gradual.
- many loci may be involved and the strength of selection required to drive this divergence can be
small (because gene flow has ceased between populations).
- under the parapatric model, the strength of selection must be greater to maintain the differences
between the populations because of the fact that they remain in contact and continue to exchange
small number of migrants each generation.
- under the sympatric model, the conditions become even more restrictive for speciation.
- this is because individuals of the two diverging groups can easily to come into contact and
reproduce.
- when they do, the genetic differences developing between the groups would be eliminated.
- most examples of sympatric speciation are highly controversial.
- from the time of the modern synthesis up until very recently, the importance of sympatric
speciation was greatly downplayed.
- most models of sympatric speciation require that at least two genetic loci be involved.
- in the model made for Rhagoletis fruit flies, one of these genes is involved in host (i.e., fruit)
recognition, the other for larval survivorship once the egg is deposited in the host.
What are evolutionary processes are involved in the speciation process?
1. ,atural selection
- this is by far the most important evolutionary process causing speciation.
- driven by different abiotic conditions (e.g., temperature, altitude) and biotic conditions (e.g.,
competitors, parasites).
- under the allopatric model, speciation results as an incidental by-product of the action of
natural selection acting in different populations over evolutionary time scales.
- there is no direct selection for speciation – this is a simply a secondary consequence of
impendent evolution.
2. Sexual selection
- Darwin recognized that species-rich groups tended to those in which strong sexual
selection may be occurring.
- this matter is only recently being given the attention it deserves.
- recently, studies have suggested that sexually antagonistic genes may play an important role in
speciation.
- in examining the source of reproductive isolation, we can broadly define two classes of genes:
those that cause sterility in hybrids and those that cause hybrids to be inviable.
- recent work in Drosophila has suggested that genes causing sterility in hybrids evolve at much
faster rates than those that affect viability.
- in fact, about 10X more genes appear to cause sterility than viability.
-sexual selection is now being considered as an “engine of speciation”
3. Random genetic drift
- may involve founder effects and genetic bottlenecks.
- not important in either parapatric or sympatric speciation but may play some (minor) role in
allopatric speciation.
- here, neutral mutations may accumulate in different geographically separated populations that
may not be neutral in hybrids.
Some generalities…
1. The magnitude of prezygotic and postzygotic isolation both increase with the time.
- this makes it difficult to assess which isolating mechanisms evolved earlier or later in the
speciation process.
- the length of time for complete reproductive isolation to evolve differs between different
groups.
- in Drosophila, it takes about 1.5 to 3 million years.
- in marine bivalves, it may take 4 to 6 million years!
2. Among recently separated groups, prezygotic isolation is generally stronger than
postzygotic isolation.
- this suggests that prezygotic isolating mechanisms play a more important role in establishing
reproductive barriers.
3. In the early stages of speciation, hybrid sterility or inviability is almost always seen in the
heterogametic sex.
- for example, D. simulans and D. mauritiana female hybrids are completely viable yet male
hybrids are completely sterile!
- this is called Haldane’s rule.
What causes postzygotic isolation?
- the underlying mechanism is called Dobzhansky-Muller incompatibility:
- consider an ancestral population that divides into two allopatric populations.
- suppose in each derived population, a different substitution occurs at two distinct loci.
Ancestral Pop:
Derived Pops:
A1A1B1B1
A2A2B1B1
A1A1B2B2
A1A2B1B2 reduced fitness
Hybrids:
- when the A2 and B2 alleles occur together in a hybrid, they reduce fitness because each
functions poorly in the presence of the other.
- this form of negative epistasis is called Dobzhansky-Muller incompatibility.
- the fixation of the A2 allele could never happen in a population that previously undergone a
fixation of the B2 allele.
- this simple model is believed to underlie hybrid inviability or sterility.
Differences between plant and animal speciation
- there is a fundamental difference between plants and animals in the likelihood of sympatric
speciation occurring by the process of polyploidization.
- polyploidization refers to the retention of extra sets of chromosomes (i.e., tetraploids,
octoploids, etc.)
- in fact, estimates of the plant species that have speciated by polyploidization range from 4070%.
- in contrast, polyploidization in animals appears to be far less common (although has been found
in some families of fishes and salamanders).
- there are two types of polyploids - autopolyploids and allopolyploids.
- autopolyploids are formed when an extra set of chromosomes are retained from a cross between
individuals of the same species (e.g., a tetraploid species may be formed from a diploid ancestor).
Species 1
(2N = 4)
x
Species 1
(2N = 4)
→
Species 2
(4N = 8)
- the tetraploid (species 2) is instantaneously reproductively isolated from the parental diploid
(species 1) because when it crosses with the latter it will produce a sterile triploid.
- allopolyploids are formed when chromosome sets from two different species are merged.
Species 1
(2N = 4)
x
Species 2
(2N = 6)
→
Species 3
(2N = 10)
- although we thought that autopolyploidy was more common than allopolyploidy, recent
molecular data suggests that this is incorrect.
- the reasons for why polyploids are much more viable in plants than in animals is unclear.
Secondary contact and reinforcement
- “secondary contact” occurs when two formerly allopatric populations meet.
- three outcomes are possible:
1. ,o interbreeding occurs
- isolating mechanisms in place – speciation completed.
2. Introgression
- no isolating mechanisms in place – the populations merge together over time.
- how often does this occur?
- difficult to say, since it would leave no hint of having happened.
3. Partial interbreeding occurs
- some isolating mechanisms in place – a hybrid zone forms (but hybrids are less fit).
- this is an extremely common outcome – hybrid zones are widespread in nature and have been
described in virtually every organismal group.
- the prevailing view is that these zones reflect secondary contact and introgression.
- whether additional isolating mechanisms readily evolve to “complete” or “reinforce” the
speciation process is controversial.
- Dobzhansky referred to this process as reinforcement – the acquisition of additional isolating
mechanisms to “complete” the speciation process.
- this process should be strongly favored by selection because it would eliminate reproductive
effort to produce inferior hybrids.
- although this argument makes sense, there is not much evidence favoring reinforcement and
many hybrid zones are known to have persisted for extremely long periods of time.
- why hasn’t selection acted to complete the speciation process?
- evidence favoring the reinforcement process has recently come from the work of Coyne and Orr
(1997) comparing 42 sister species of Drosophila.
- they examined the degree of premating isolation among species pairs and related it to the degree
of genetic divergence (estimated from allozymes).
- a clear difference emerged between sister species that were sympatric and those that were
allopatric.
- for the sympatric species pairs, Coyne and Orr observed a much higher degree of prezygotic
isolation at low levels of genetic divergence than shown by the allopatric species pairs.
- this is exactly the pattern predicted by reinforcement.
- this study has breathed new life into an old problem and many researchers are actively
investigating reinforcement in many species groups.
Ecological speciation in sticklebacks
- about 8 lakes in southern British Columbia have two distinct species of sticklebacks.
- one is a limnetic species that is small, slim, and lives high in the water column.
- it feeds by filtering microscopic plankton using long gill rakers.
- the other is a benthic species that inhabits the shallow water around the shoreline.
- it feeds on a variety of invertebrates and insect larvae.
- the benthic species is considerably larger than the limnetic.
- the textbook states that each limnetic and benthic species pair evolved from a marine
stickleback ancestor after the last ice sheets receded (about 10,000 – 15,000 years ago).
- although this is correct, it does not account for the accepted model of their divergence (and
seems to imply a sympatric origin for each pair).
- the limnetic and benthic species pair did evolve independently in each lake (a good example of
parallel evolution) but did so because of two separate invasions.
- the first invasion occurred about 10,000 years ago by a marine stickleback that adapted to life in
the new freshwater enironment.
- a second invasion occurred in these lakes to reintroduce the marine species a second time.
- it is from this second invasion that the limnetic species is thought to have evolved.
- why do we believe this?
- there are three lines of evidence.
- first, only low elevation lakes possess limnetic and benthic species pairs.
- second, cores from lakes with limnetic and benthic species pairs show evidence of salt water
influx (e.g, clams, etc.).
- third, higher elevation lakes have neither limnetic and benthic species pairs nor evidence of salt
water influx.
- therefore, there are no known cases where the limnetic and benthic species pairs have evolved
de novo in any lake.
- the initial genetic divergence that gave rise to each species pair evolved allopatrically.
- this does not deny the rapid diversification of these species but does undermine their presumed
sympatric origin.