Speciation
most important problem in evolutionary biology
- change over time
- diversification
Species concepts
Mechanisms of speciation
Species Concepts
Mayden (1997)
22 different species concepts
species as categories -- taxa
species as evolutionary groups -- “smallest
independent evolutionary unit”
importance -- conservation of biological diversity
understanding the process of diversification
Biological Species Concept -- Ernst Mayr (1947)
“Species are actual or potentially interbreeding natural
populations which are reproductively isolated from
other populations”
emphasizes:
genetic exchange within species
reproductive isolation between species
can be difficult to apply
and, doesn’t apply to many species:
asexual species --
bacteria, fungi, many invertebrates
and plants
hybridizing species -- wolves and coyotes; cottonwood
and balsam poplar
fossil species
Phylogenetic Species Concept -- Joel Cracraft (1989)
“An irreducible (basal) cluster of organisms diagnosably different
from other such clusters, and within which there is a parental
pattern of ancestry and descent”
species are monphyletic
groups
can be applied to any
type of organism
can be difficult to
implement
difficulties with matching
gene trees to speciation
events
Morphospecies Concept
fossil species
problems of cryptic species because of limited characters
Geographical classification (passJ)
allopatric
vicariance
founder event
parapatric
sympatric
Classical model of allopatric speciation
isolation of populations
allopatry
genetic divergence of populations
allopatry
development of reproductive isolation
when populations come back into contact
(secondary contact and reinforcement)
sympatry
geographic isolation due to range splitting -- vicariance
populations may diverge due to:
natural selection
sexual selection
(genetic drift)
type of divergence may be pre-mating or post-mating or both
Vicariant speciation in
snapping shrimp
Isthmus of Panama closes ~3 mya
Caribbean, Pacific populations
both pre-mating and post-mating
divergence
geographic isolation due to a founder event
founder population is genetically different from source population;
genetic drift is important at the start of the process
divergence via:
natural selection in a novel environment
sexual selection
type of divergence may be pre-mating or post-mating or both
Patterns of speciation in Hawaiian Drosophila are consistent
with founder events
outcomes of divergence in allopatry
insufficent divergence ---> fusion
reproductive isolation due to assortative mating within
populations ---> speciation
mating between populations leading to a hybrid zone
hybrid fitness
hybrid zone
eventual outcome
lower than
parental forms
narrow, shortlived
reinforcement
equal to
parental forms
wide,
persistent
parental populations
coalesce
greater than
parental forms
ecotone
new habitat
stable hybrid zone,
new species
Classical model of allopatric speciation
isolation of populations
allopatry
genetic divergence of populations
allopatry
development of reproductive isolation
when populations come back into contact
(secondary contact and reinforcement)
sympatry
Not unique to allopatric speciation
*first two stages frequently happen in ‘sympatry’
differentiation despite gene flow due to selection
reproductive isolation is a consequence of selection on
ecological attributes
Ecological speciation in three-spined
sticklebacks
Rundle et al. 2000 Science 287:306
pairs of species in freshwater lakes;
independently derived from a
marine stickleback species
benthic form -- large, heavy-bodied;
feeds on invertebrates in the
near-shore habitats
limnetic form – slender-bodied;
feeds on plankton in open water
Predict: limnetic forms from different lakes should not be reproductively
isolated from each other
limnetic forms from one lake should be isolated from benthic
forms from a different lake
species pairs from three different lakes
different lakes
same lake
Natural selection, sexual
selection selection and
speciation in the cichlids
of Lake Victoria
Verheyen et al. 2003
Science 300:325
Lake Victoria -- more than 500 species of haplochromine cichlids
morphological, ecological, and behavioral diversity
Lake Victoria cichlids are
a monophyletic group
most closely related to
taxa from Lake Kivu
algal grazer
insect eater
piscivore
algal grazer
Sexual selection drives
speciation in African
great lakes cichlids
Couldridge and Alexander 2002 Behavioral Ecology 13:59
Pseudotropheus zebra
complex of at least four species (Lake Malawi)
differ in color pattern; similar in other morphology, ecology, behavior
Test for assortative mating
female preference with choice (conspecifics and heterospecifics)
female preference without choice (heterospecifics only)
C P. callainos
pale blue, no bars
R P. zebra “red dorsal”
pale blue; dark blue
bars; orange
dorsal fin
G P. zebra “gold”
pale orange, faint
brown bars
L P. lombardoi
yellow, 5 vertical
black bars
Predict: 1) in choice tests, females will prefer conspecific males
2) in no choice tests, females will prefer the heterospecific
male whose color pattern is most similar
*
*
*
*
C P. callainos
pale blue, no bars
R P. zebra “red dorsal”
pale blue; dark blue
bars; orange
dorsal fin
G P. zebra “gold”
pale orange, faint
brown bars
*
*
*
*
L P. lombardoi
yellow, 5 vertical
black bars
Disruptive selection and speciation
in red crossbills, Loxia curvirostra
highly specialized -- seeds of coniferous trees (seeds retained in cones)
use the crossed bill to extract seeds from within the cone
extraction efficiency depends on bill shape and palate structure
bill structure and cone structure affect feeding performance
---> no generalist crossbill
nine different call types; seven are specialized on different species of conifers
Benkman 2003 Evolution 57:1176
detailed study of one population in southern Idaho
feeds on Rocky Mountain lodgepole pine (Pinus contorta latifolia)
estimated form of selection on bill shape (bill depth)
relationship between bill depth and fitness (survival)
fitness surface based on feeding performance (bill depth
and palate structure) for five species
Selection on bill depth is
stabilizing
Selection and speciation
Natural Selection for different feeding methods or
habitat preferences
Sexual Selection for mate preferences
Hybrids do poorly because they do not work well in
the environment (physical or social).
They may function properly as organisms
i.e. viable and fertile
What are the requirements for this to work?
Strong selection
Little genetic exchange/assortative mating
Predictions
Prerequisite of close linkage/pleiotropy between the traits
of ‘mating’ and ‘performance’
or,
Recombination will erode weaker associations
leading to no speciation
Genetics of speciation -- performance and habitat preference
in pea aphids
Via 2002
two host races/incipient species -- alfalfa and clover
known trade-off between performance on clover and alfalfa
reaction norms
mean fitness of clones
tested on both hosts
Genetics of speciation -- performance and habitat preference
in pea aphids
Via 2002
two host races/incipient species -- alfalfa and clover
known trade-off between performance on clover and alfalfa
what is the genetic architecture of this trade-off?
are genes for performance independent of genes for
habitat choice/assortative mating?
negative genetic correlation:
pleiotropy or LDE of closely linked loci
vs. LDE of unlinked loci
QTL analysis
Performance
Acceptance and
Performance on alfalfa
Acceptance and performance on clover
Intrinsic postmating incompatibility
Drosophila
frogs
Lepidoptera
birds
Post
Lepidoptera
Pre- plus post
Hybrid sterility and inviability evolve gradually; positively correlated
with the time since divergence -- gradual accumulation of
deleterious epistatic interactions between species
Hybrid sterility evolves faster than inviability
Haldane’s Rule: if hybrid sterility or inviability is present in only one
sex of F1 offspring, it will be the heterogametic sex
For Drosophila it is males--for Lepidoptera it is females
Haldane’s Rule: if hybrid sterility or inviability is present in only one
sex of F1 offspring, it will be the heterogametic sex
inviability due to lethal incompatibilities between autosomal and X-linked loci
dominance theory: hybrid incompatibilities are partially recessive
XX hybrids are heterozygous and protected
X Y hybrids express all X-linked recessives
faster-male evolution:
- sexual selection drives rapid divergence of male fertility
factors ---> hybrid male sterility
- spermatogenesis is inherently more sensitive to perturbation
Species are evolutionarily independent groups. A species is often defined as
a group of populations that are capable of interbreeding, but this definition
applies best to diploid, sexually reproducing taxa. Populations which are
phenotypically or ecologically distinct, yet regularly interbreed, or species
that reproduce largely asexually may still be valid species.
The process of adaptive divergence that leads to speciation may occur either in
allopatry or sympatry.
Speciation is a result of divergent natural (ecological) or sexual selection. Genetic
drift may accelerate the process of divergence during founder events.
Reproductive isolation between species may result from assortative mating
(prezygotic) or from hybrid sterility/inviability (postzygotic).
Haldane’s rule is a general description of the early stages of speciation.
Genetic correlations for performance in different environments and for habitat
choice may facilitate the rate at which divergence occurs.