1 Speciation: Definitions, Mechanisms, Theories, Data 1. Species

Speciation: Definitions, Mechanisms, Theories, Data
1. Species Concepts
There is no clear consensus among biologists on how to define a “species”. Many definitions
or “species concepts” have been proposed, each with advantages and disadvantages.
a) Biological – Groups of interbreeding natural populations that are reproductively
isolated from other such groups (proposed by E. Mayr). Con: How can you apply to
asexual or extinct organisms?
b) Morphological – A group of organisms sharing a unique combination of physical
characteristics. Con: A species may be morphologically diverse (e.g., dogs) or distinct
species may be morphologically indistinguishable (“cryptic species”).
c) Evolutionary (cladistic) – A group of organisms sharing a unique, common
evolutionary history. Con: Evolutionary history is typically not known, ideas may
change with further research.
d) Genealogical – A group of organisms whose members share an exclusive
genealogical relationship, composite over many genes. Con: Requires extensive
phylogenetic data.
e) Genic – A group of organisms with particular adapted gene(s) that do not mix with
other such groups, although other genes may be exchanged. Complete reproductive
isolation is not required. Con: Requires extensive knowledge of genetics/adaptation.
f) Operational – bacterial strains with over 70% similarity in genomic DNA sequence or
over 97% similarity in 16S rRNA sequence are considered the same species. Con:
arbitrary similarity cut-off, can be conflicts among sets of species.
The Biological Species Concept (BSC) is probably the most popular and the most practical
for experimental studies of speciation genetics.
2. Biogeographic Speciation Models
a) Allopatric Speciation - two populations are physically separated, evolve
independently and diverge. This is the dominant view of how speciation occurs.
Example: North American bird species – often eastern and western sister species.
b) Sympatric Speciation - one species becomes two without physical separation. This
has received a lot of attention because it is difficult to envision how speciation can
occur without some type of physical separation. Thus, theorists have come up with
some very clever scenarios that allow sympatric speciation to occur. All rely on
physical or behavioral traits being linked to mate selection. Some examples:
Disruptive selection: Suppose natural selection favors fish with small body
size (feed on small prey) or large body size (feed on large prey). Medium
sized fish are disfavored. Disruptive selection will lead to two distinct
phenotypes. If there is assortative mating between types, this can lead to two
reproductively isolated populations that differ in phenotype and ecological
niche, eventually leading to speciation.
Pollinator isolation: For example, there are two sister species of flowers
(genus Mimulus), one pollinated by bees and the other by humming birds. The
species’ flowers have diverged to match the pollinator’s preference, which
leads to reproductive isolation.
Sexual selection: If males are polymorphic for phenotypic traits (such as body
coloration in Cichlid fishes) and females are polymorphic for mate choice and the two traits are linked - then sympatric speciation is possible.
Ecological shift: An example is the apple maggot fly (Rhagoletus). This fly
lived on Hawthorne trees in New York State until apple trees were introduced
in the mid-1800s. Following introduction, some flies shifted to apple, while
others remained on Hawthorne. There is a genetic basis to host tree preference.
Furthermore, the flies mate on their host plants – so there is assortative mating
between flies with different host preferences.
c) Parapatric Speciation - two populations are separated, but gene flow is not completely
blocked. This is a combination of the two above models, and represents a situation
often observed in nature. The ranges of two species overlap in a “hybrid zone.” If the
hybrids are less fit, there may be reinforcement to prevent hybridization. Or perhaps
some genes are exchanged and others are not. This relates to the “Genic” species
3. The Genetics of Speciation
Bariers to reproduction may be:
Pre-mating (pre-zygotic) – behavioral, geographical, physical, temporal
Post-mating (post-zygotic) – hybrid sterility or inviability
Pre-mating barriers may evolve to avoid post-mating incompatibilities (“reinforcement”).
Many genetic studies focus on post-zygotic incompatibilities.
A simple model of genetic changes leading to hybrid incompatibilities is known as the
Dobzhansky-Muller 2-locus model. Here, one assumes that an ancestral species has been
separated into two independent populations. Over time, mutations will occur independently in
each population, and some will become fixed (that is, reach a frequency of 100% in the
population). Within each population, the fixed mutation must be compatible with the rest of
the genome. However, there is no guarantee that the mutations that fixed independently in
each population will be compatible with each other in a hybrid.
Dobzhansky-Muller 2-locus model
(A and b compatible)
(a and B compatible)
(A and B not compatible)
It is important to note that positive selection is not required for speciation to occur under the
DM model. Incompatible loci may result from the fixation of mutations by random genetic
drift in isolated populations. However, positive selection can speed up the process, because
positively-selected mutations will become fixed faster than neutral mutations under drift.
4. Haldane’s Rule
In the F1 hybrids of two species: If one sex is absent or sterile, it is the heterogametic sex.
In most organisms used for genetic experiments, males are heterogametic (XY) and it is
very common to observe sterile hybrid males. However, in birds and butterflies, females
are heterogametic (ZW) and are more affected by incompatibilities.
Two hypotheses to explain Haldane’s rule:
a) Dominance – If an X-linked incompatible allele is recessive, it will be “hidden” in the
female (homogametic) hybrid, but exposed in the male (heterogametic) hybrid.
b) Faster male evolution – genes involved in male reproduction evolve faster than other
genes (female reproductive genes, genes encoding enzymes or structural proteins –
“housekeeping” genes). This means that more mutations become fixed in male
reproductive genes over a given time period, leading to more Dobzhansky-Muller
incompatibilities in male reproduction. Faster male evolution may be caused by
sexual selection, which is typically much stronger in males than in females. Note that
this explanation should mainly apply to hybrid sterility and can only explain
Haldane’s rule in species where males are the heterogametic sex.
5. Experimental Results
a) Using mosquitos to test the causes of Haldane’s rule
Mosquitos of the genus Anopheles have the “typical” XY sex determination system,
while those of the genus Aedes have single-locus sex determination. The Aedes X and
Y chromosomes differ only at the sex-determination locus and recombine over the
rest of the chromosome. For practical purposes, the males and females can both be
considered XX.
The results from Anopheles hybridizations were compared with those of Aedes
On the dominance theory, Anopheles should follow Haldane’s rule for both sterility
and viability, but Aedes should not. If there is faster male evolution, Aedes should
obey Haldane’s rule for male sterility.
The results suggest that both dominance and faster male evolution contribute to
Haldane’s rule: Anopheles follows the rule for both sterility and viability. Aedes
follows the rule only for male sterility.
b) “Evolution Canyon” (Mt. Carmel, Israel)
The North and South-facing slopes have extremely different environmental
conditions, despite being only 400 m apart at the top and 100 m apart at the bottom.
The South-facing slope (SFS) is much hotter and drier. Although Drosophila flies
may traverse several kilometers per day, the D. melanogaster populations living on
the two slopes differ in a number of morphological, metabolic, behavioral, and
genetic characteristics (body size, heat tolerance, mate preference, microsatellites,
Hsp70 alleles). Thus, this looks like a case of differential adaptation of two parapatric
populations and potential incipient speciation.
c) Microbe-induced Speciation?
Wolbachia are a type of bacteria that infect many species of insects and may have
dramatic effects on their reproduction. The bacteria are transmitted vertically (from
mother to offspring) in the cytoplasm of the egg. They are not transmitted from father
to offspring because the bacteria are excluded from sperm. Wolbachia use an
unknown mechanism to render infected males sterile unless they mate with infected
There are two wasp species that are infected by different strains of Wolbachia. The
two species cannot hybridize to form viable offspring. However, when the wasps are
cured of Wolbachia with antibiotics, they can form viable, fertile hybrids. Thus,
Wolbachia appears to be the cause of reproductive isolation between the two species
and could represent a mechanism for speciation.
Male W1 Offspring None
W2 None Offspring
Male W1 Offspring Offspring
W2 Offspring Offspring
No antibiotics
With antibiotics
d) Single-gene speciation in snails
In snails, a single maternal gene controls the “handedness” of the shell.
RR or Rr = right handed or “dextral” (dominant), rr = left-handed or “sinstral”.
Snails are hermaphrodites with reciprocal mating (that is, they mate as males and
females simultaneously). However, it is physically very difficult or impossible for two
snails of a different “handedness” to mate with each other. Thus, there can be instant
reproductive isolation between snails with different handedness.
Presgraves, D. C., and H. A. Orr, 1998 Haldane's rule in taxa lacking a hemizygous X. Science 282: 952-954.
Michalak et al., 2001 Genetic evidence for adaptation-driven incipient speciation of Drosophila melanogaster
along a microclimatic contrast in "Evolution Canyon," Israel. Proc. Natl. Acad. Sci. USA 98: 13195-13200.
Korol, A. et al., 2006 Drosophila flies in "Evolution Canyon" as a model for incipient sympatric speciation.
Proc. Natl. Acad. Sci. USA 103: 18184-18189.
Bordenstein, S. R., et al., 2001 Wolbachia-induced incompatibility precedes other hybrid incompatibilities in
Nasonia. Nature 409: 707-710.
Ueshima, R., and T. Asami, 2003 Single-gene speciation by left-right reversal. Nature 425: 679.