Species Radiations

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Species Radiations

• Readings
• Grant Grant (2002) Science paper

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Species radiations The opposite of extinction is
radiation speciation diversifying a taxon. One
example was introduced at the beginning of the
previous slide set the radiation of Darwins
finches on the Galapagos. The Galapagos islands
are a group of 16 major islands plus an equal
number of smaller islets located on the equator
about 1000 km west of Ecuador.  The archipelago
was formed following volcanic eruptions of the
seafloor ca. 3 - 5 million years ago.  The
islands, because of their remoteness from
mainland sources of plants and animals, have a
relatively impoverished biota. 
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Galapagos Islands Most islands are not occupied
Darwin visited the islands in 1830 Cocos Island
is 600km NE
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26 species of land birds occurred naturally on
the Islands before human introductions 13 of
these are finches. The islands also support 4
mockingbird, 2 flycatcher, 2 owl, 1 hawk, 1 dove,
1 cuckoo, 1 warbler and 1 martin species (Pianka
1983) The island finches belong to a distinct
subfamily of finches, endemic to the Galapagos
and Cocos Island (Costa Rica).  Cocos Island is
several hundred km north of the Galapagos and
about the same distance from the mainland. It
supports only 1 finch species, the Cocos Island
finch Pinaroloxias inornata. The Cocos finch is a
generalist feeder.
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On the Galapagos Islands, adaptive radiation has
resulted from geographic isolation and reduced
gene flow among islands. Three distinct
genera (Geospiza, Camarhynchus and Certhidea)
occur on the islands.  Members of these genera
differ in where they forage, how they forage, and
what they eat. Genus Geospiza includes 6
ground-foraging species with broad beaks that
crush different species and/or sizes of seeds, or
use flowers of Opuntia cactus. 
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Darwin's finches (classical view)
Cocos finch
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A more modern view... (Sato et al .1999) PNAS
based upon mtDNA sequences
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A more modern view... (Sato et al .1999) PNAS
based upon mtDNA sequences

• Warbler finch may be the ancestral species, not
  the Cocos finch, which groups with the tree
  finches.
• Vegetarian finch most closely related to warbler
  finch
• tree and ground finches remain separate

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Finch diversity by island
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The 6 species of Camarhynchus finches forage in
trees, have narrower beaks, and eat either
vegetation (1 species) or different sizes of
insects.  C. pallidus uses a stick or cactus
spine to probe for insects.  
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Another genus has one species, Certhidea
olivacea, called a 'warbler-finch'. Beak lengths
and depths vary widely from island to island, and
in some cases, provide evidence for competitive
displacement On islands (Abington,
Bindloe, James, Jervis, Albemarle, Indefatigable,
Charles, Chatham) where Geospiza fuliginosa and
G. fortis occur sympatrically, they tend to have
widely divergent beak depths. Only one of these
species is on each of Daphne and Crossman.  The
beak morphologies are very similar when the
species occur in isolation.
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(No Transcript)
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Before it can be confirmed that character
displacement has occurred, 4 conditions must be
met
1) the change in mean character state in areas of
overlap should not be predictable from variation
within areas of overlap/isolation 2) sampling
should occur at more than one set of locations
to eliminate local variation effects 3)
Heritability of the feature must be high if
genetic variation is thought to underlie
variation in the feature, and if it is to be
passed to subsequent generations 4) Evidence
must be presented to demonstrate that competition
occurs and that the measured feature has
relevance to competition among groups
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Conditions 1 and 3 have been demonstrated The
variation observed in G. fortis in isolation on
Daphne greatly exceeds that observed on other
islands.  Heritability of the trait for beak
morphology which can range from 0 (no relation
between parental and offspring morphology) to 1
(absolute relationship) has been estimated as
0.82. 
There is good tentative evidence for criterion 4.
Peter and Rosemary Grant recently demonstrated
that co-occurring finches diverged in beak
morphology after a drought which greatly reduced
seed abundance, relative to their respective beak
shapes prior to the drought. There is, however,
no way to deal with criterion 2 since there is
only one Daphne and one Crossman.  Satisfying
this requirement would necessitate observing the
same pattern on other islands like Daphne and
Crossman. 
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G. fortis on Daphne Major (Grant Grant 1993,
Proc. R. Soc. Lon. B)
rainfall on Daphne Major
seed size (white) and hardness (black)
small seeds solid large seeds open
relative abundance of small seeds increased
dramatically (right) following El Nino in 1983
(left).
fortis (top), scandens (bottom)
Strong selection for fortis, which feeds on small
seeds, over scandens, which feeds on rare cactus
seeds, following drought after 1983
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G. fortis on Daphne Major (Boag Grant 1981,
Science)
PC 1 (morphology)
popn size
seed size
seed abundance

• 1500 birds banded and studied between 1975-78
• regular rainfall (large finch populations) until
  1977, when only 24mm rain fell. fortis did not
  breed and 85 decline in population (A) seed
  abundance declined (B), big males survived best
  (C), corresponding with decline of small seeds (D)

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The distributions of individual species also
suggest competition has occurred among the
finches Two closely related taxa, G. fortis and
G. conirostris, have completely different
distribution patterns and never co-occur. G.
difficilis is found on very few islands located
at different ends of the archipelago, suggesting
that it has had opportunity to colonize islands
in between. Grant and Schluter (1984) attributed
its rarity and absence on additional islands to
competition from other finch species. 
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Geospiza bill morphology. Both geographically
restricted species (conirostris, difficilis) have
bill depth similar to widespread species (fortis,
fulignosa)
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G. difficilis is found on 4 widely separated
islands and extinct on 4 others. It co-occurs
with G. fuliginosa on large central islands
(presumably with large habitat area supporting
large populations), but does not co-occur on
smaller central or small outlying islands. Grant
and Schluter used statistical comparisons to
suggest that these species co-occur much less
than one would expect by chance alone.
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Grant Grant (2002) Science paper

• studies the same populations of G. fortis
  (medium ground finch) and G. scandens (cactus
  finch) on Daphne Major for 30 years
• survival of marked and measured individuals
  measured each year
• 6 traits studied were reduced by Principal
  Components Analysis, which break down as body
  size, beak size and beak shape

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If species were not changing, each measure should
have stayed within its original 95 confidence
interval (horiz. lines). Clearly this is not
happening. scandens converged on fortis'
morphology
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1. body beak sizes selected more than beak shape
2. species differed in net selection direction on
   size traits (fortis in both directions with equal
   frequency, scandens selection repeatedly favoured
   large body size and never small beak size)
3. unidirectional selection (up to 3 yrs) occurred
   in both species
4. selection events in the species were not
   synchronized except in late '70s during a drought
5. each of these studied traits was highly
   heritable, so evolution followed for fortis (4
   body size

3 beak size, 1 beak shape) and for scandens (2
body size, 5 beak size)
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Predicted and observed evolutionary responses in
beak size and shape are determined by the product
of selection differentials and heritabilities
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Proportion of hybrids and backcrosses are higher
in scandens than in fortis (see b), thus new
variation introduced to the population should
follow the same pattern
Mean (a) and variance (b) of beak shape changes
more in scandens than fortis due to presence of
hybrids and backcrosses (white bars). Result due
to higher mate competition in fortis (11 sex
ratio) after a drought had killed many scandens
females (male bias afterwards).
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The Galapagos finches experienced adaptive
radiation, a process whereby the species
diversified to exploit a wide variety of
available niches.  As in the following cases of
the Hawaiian honeycreepers and cichlid fishes of
the African Great Lakes, closely related taxa
co-exist by exploiting different habitats. If
individuals with similar niches practiced
assortative mating, in which they preferentially
mate with individuals sharing similar traits or
habits, then sympatric speciation is possible.
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Aging the Hawaiian Islands
Fleisher et al. (1998) Mol. Ecol.
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Hawaiian honeycreepers These birds experienced
much greater adaptive radiation than Darwin's
finches, though, sadly, many of the taxa have
been driven extinct due to introduction of
diseases, other passerine birds and mammals, and
destruction of habitat.  On Laysan Island
introduced rabbits and a windstorm destroyed
vegetation resulting in the extinction of the
Laysan honeycreeper. Bird pox virus and avian
malaria (introduced to the Hawaiian islands by
mosquitoes on ships in 1826) have caused sharp
declines in Drepanidid species, including the
honeycreeper.
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wide diversity, some now extinct (E)
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beak shape highly variable and highly adapted to
feeding mode
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Origin of the Honeycreepers

• Johnson et al. (1989) used starch gel
  electrophoresis to study 8 genera (9 species) of
  honeycreepers
• they are a monophyletic group (only one ancestor)
• the ancestral species colonized the Hawaiian
  archipelago 7-8 million yr ago
• this agrees with the emergence of Nihoa (now
  largely submerged) but predated the island of
  Kauai (5 MYBP)
• Oreomystis and Paroreomyza are the oldest and
  most diverse lineages
• youngest lineages are the nectar feeders and
  thick billed finch types

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Views of honeycreeper phylogeny based on mtDNA
(top) and allozymes (20, variable) (bottom)
true creepers
Time difference between island formation dictates
genetic distance between species
Fleisher et al. (1998) Mol. Ecol.
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Time difference between island formation dictates
genetic distance between species
Honeycreepers Hawaiian
Drosophila sequence divergence rate 0.016 per
Million/yr 0.019 per Million/yr
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• Currently, honeycreepers occur primarily at
  altitudes above 600 m on the main islands and on
  several smaller remote islands in the NW part of
  the archipelago.
• Mosquitoes, by contrast, occur primarily below
  600 m, and overlap very little with the
  honeycreepers.
• At the lower altitudinal end of the honeycreeper
  species ranges, between 2 and 7 of individuals
  have avian malaria. 
• Rats have also played a large role in species
  extinctions.

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• in total, 28 of 53 known species are extinct (34
  known from historical records, 19 from fossil
  records)
• 18 of the remaining species are endangered
• 9 extinctions have occurred since introduction of
  malaria to the islands. Of these, 6 occurred on
  Lana'i, Moloka'i and O'ahu. These islands have
  been radically modified by humans, thus habitat
  destruction appears to have played a large role.
• Behaviour may have affected 2 large,
  nectar-feeding Drepanidid species driven extinct
  and 2 smaller ones extirpated ('akoekoe and
  'i'iwi) on some islands.
• The rare 'akiapola'au, a specialized insectivore,
  has become endangered because it lives primarily
  in large koa trees koa trees have been widely
  harvested for furniture lumber. 

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• Another endangered species, the palila, a
  granivore, exploits seeds of one tree, the
  mamane. This tree has been adversely affected by
  introduced goats and sheep, thereby endangering
  the bird.
• Honeycreepers are endangered because of their
  extreme specialization (habitat or food), which
  itself is a result of dramatic adaptive
  radiation. This problem may be compounded by
  introduced diseases, mammals, and exotic birds.

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What's the Honeycreeper's Future?Benning et al.
(2002) PNAS

• habitat loss began with the Polynesian colonists
  (900-1000 yrs ago), who cleared low elevation and
  seasonally dry forest
• European colonists brought new agricultural
  technology, domesticated cattle
• hunting, beginning with Polynesians, and
  introduction of dogs and rats that preyed on
  nesting birds. These predators were followed by
  mongoose, cats and 2 more rat species
• introduction of mosquitoes and of avian pox, and
  more recently avian malaria, had the greatest
  consequences

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Temp. lt13C is critical to prevent malaria
infection. In Hanawi Forest (Maui), a 2C
increase would cut this zone area by half (665 to
285Ha).
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low mosquito risk zone, Hanawi, Maui
low mosquito risk zone, Hakakau Refuge, Hawaii
(low risk areas declines from 3120 to 130 HA)
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Alakai Swamp, Kauai. No area currently below
13C, area of possible high risk moves up 300m.
Must focus on disease prevention in remaining
honeycreeper populations.
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Hawaiian Drosophila

• More than 900 endemic species, each typically
  restricted to one island.
• Speciation of these flies is also speculated to
  have occurred as a result of adaptive radiation. 
  The speciation mechanism is not entirely clear,
  though two main models are
• 1) Mayr's founder effect model
• 2) Brian Charlesworths model of adaptive
  divergence under new selective pressures 
• molecular data suggest separation of Hawaiian
  lineage from mainland lineage between 10-32 MYBP

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Hawaiian Drosophila
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Mayrs model a few new colonists to an island
represent only a small fraction of the total
Drosophila gene pool.  Genetic drift then
results in dramatic 'peak shifts' in the genome
of colonizing species relative to the parental
stock (so long as gene exchange is precluded). 
This genetic change in the population would
occur very rapidly and would be driven by local
selective pressures in a relatively homogeneous
environment. 
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Genetic variation is far more pronounced if you
start with small as opposed to large populations
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Hampton Carson modified this model
slightly. Certain loci form strong epistatic
relationships (synergistic effects caused by
multiple loci) and a 'closed variability system'.
For example, in fruit flies, genes controlling
mate recognition and behaviour may form such a
closed variability system' in which females will
recognize only specific behaviours or
morphologies when preparing to mate. These blocks
of genes may become destabilized during founding
events. Recombinants that previously had low
fitness may now thrive, bringing the new
population to a new  'adaptive peak'.
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Templeton modified the model differently,
suggesting that change in allelic frequencies for
a few key genes (owing to genetic drift) could
precipitate changes in modifier loci in the new
environment, leading to a new co-adapted state of
the character.  One evidence Kaneshiro has
determined that some species differ only by one
mutation. This mutation modified the behavioural
repertoire of males during mating rituals. 
Derived species females would recognize the
ritual and mate with the mutated individual,
whereas ancestral females (the parental species)
would not. The species were behaviourally
(sexually) isolated from one another.
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Charlesworths model founding may not be the
impetus for speciation it may occur as a result
of adaptive divergence from the parental stock
under a new regime of selective
pressures.  Newly colonized islands ? new
environmental conditions ? new selection
pressures ? divergence from parental stock
Problem for both hypotheses immunological
tests with Drosophila suggested that the flies
were far older than the islands.  If this were
so, how could all of these endemic species occur
on the islands? Where did they come from?
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Colonization events (direction and number) for
Hawaiian Drosophila