Species Radiations

1. Species Radiations Readings: Grant & Grant (2002) Science paper

2. 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 Darwin’s 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. 

3. Galapagos Islands: Most islands are not occupied; Darwin visited the islands in 1830; Cocos Island is 600km NE

4. 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.

5. 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. 

6. Darwin's finches (classical view) Cocos finch

7. A more modern view... (Sato et al .1999) PNAS based upon mtDNA sequences

8. 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

9. Finch diversity by island

10. 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.  

11. Another genus has one species, Certhideaolivacea, 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.

13. 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

14. 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. 

15. 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

16. 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)

17. 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. 

18. Geospiza bill morphology. Both geographically restricted species (conirostris, difficilis) have bill depth similar to widespread species (fortis, fulignosa)

19. 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.

20. 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

21. 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

22. body & beak sizes selected more than beak shape • 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) • unidirectional selection (up to 3 yrs) occurred in both species • selection events in the species were not synchronized except in late '70s during a drought • 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)

23. Predicted and observed evolutionary responses in beak size and shape are determined by the product of selection differentials and heritabilities

24. 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 (1:1 sex ratio) after a drought had killed many scandens females (male bias afterwards).

25. 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.

26. Aging the Hawaiian Islands Fleisher et al. (1998) Mol. Ecol.

27. 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.

28. wide diversity, some now extinct (E)

29. beak shape highly variable and highly adapted to feeding mode

30. 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

31. 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.

32. 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

33. 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.

34. 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. 

35. 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.

36. 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

37. Temp. <13°C is critical to prevent malaria infection. In Hanawi Forest (Maui), a 2°C increase would cut this zone area by half (665 to 285Ha).

38. low mosquito risk zone, Hanawi, Maui low mosquito risk zone, Hakakau Refuge, Hawaii (low risk areas declines from 3120 to 130 HA)

39. Alakai Swamp, Kauai. No area currently below 13°C, area of possible high risk moves up 300m. Must focus on disease prevention in remaining honeycreeper populations.

40. 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 Charlesworth’s model of adaptive divergence under new selective pressures  • molecular data suggest separation of Hawaiian lineage from mainland lineage between 10-32 MYBP

41. Hawaiian Drosophila

42. Mayr’s 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. 

43. Genetic variation is far more pronounced if you start with small as opposed to large populations

44. 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'.

45. 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.

46. Charlesworth’s 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?

47. Colonization events (direction and number) for Hawaiian Drosophila