1 Macroevolutionary Processes—Radiations

2 Major Speciation ModelsAncestor B A Allopatric C B (island) A A’ Founder A A’ A” B Phyletic gradualism (ancestor dies out)

3 Concepts Involving RadiationsDefinition of “radiation”—relatively rapid diversification of an initial ancestral population into several derivatives (species) Often associated with opening of a new geographic area or set of new niches (e.g., ecological, behavioral, nutritional) Often accompanied or provoked by one or more novelties/innovations

4 Concepts Involving RadiationsCharacter displacement—one species affects direction of evolution or at least local behavior, in one or more competitors, not often explicitly demonstrated but often implicitly invoked in studies of radiations Parallelisms—multiple independent origins of similar traits within lineages or among closely related lineages is often compelling evidence of a radiation

5 Coevolutionary RadiationIntimate association with and parallel speciation in different organismal lineages Must demonstrate closely correspondent diversification patterns between organism groups; often revealed by congruent molecular phylogenies and tight host-user relationships Generally demands sole utilization of one host by an organism (no generalist behavior) e.g., figs and fig wasps e.g., yuccas and yucca moths

6 Adaptive Radiation “The rise of a diversity of ecological roles and attendant adaptations in different species within a lineage" (Givnish and Sytsma) Term “adaptive radiation” has been recently loosely applied to all bursts of diversification; attempts being made to restrict definition Does not always result in large species numbers or depend on a key innovation

7 Adaptive Radiation Correctly defined examples require empirical evidence: Adaptive value of phenotypic traits Comparative methods—distantly related, ecologically similar species show convergent form, physiology or behavior Functional analyses—functional significance of traits (e.g., stomata) Populational studies—phenotypic traits linked to survivorship and reproduction Environmental sorting of different phenotypic forms, tracking of multiple new niches/adaptive zones by sister taxa; similar phenotypic traits and occupation of “equivalent” habitats by non-sister taxa

8 Adaptive Radiation Examined (or at least postulated) most intensively in oceanic islands Could further subdivide examples Diversification within one habitat—e.g., pollinator exploitation Diversification across habitats—e.g., classic AR Examples later on

9 Adaptive Radiation Adaptive radiation still commonly assumed prior to investigation; results then used to characterize “an example of adaptive radiation”—circular reasoning!! Few studies have adequately demonstrated divergence in both phenotypic (e.g., morphological, anatomical) traits and ecological differentiation among sister taxa

10 Adaptive Radiation Few studies have adequately investigated the evolution of derivative taxa relative to the sister group (nearest relative[s]) Extraordinarily few groups have been investigated intensively for comprehensive information on evolutionary processes, relevant speciation models, isolation mechanisms, microevolutionary (genetic) processes, etc. Most studies have focused on island groups—easier to work with and get funded, sexier; but many of the same processes should hold for continental groups

11 Molecular Data in AR StudiesUse of phenotypic traits to reconstruct phylogeny of a group and to interpret phenotypic changes is controversial, considered by many to be circular reasoning Molecular markers provide a more "neutral" data set from which to generate a phylogeny Molecular phylogeny can be used to infer relationship of morphological traits, ecological diversification, divergence in feeding behavior, etc., and can be used as starting point for investigating molecular/developmental basis of traits

12 Evolution in African CichlidsSeveral distinctive groups, many very different looking species in each, with divergent feeding strategies within lakes Several hundred cichlid species in each lake, most endemic to one lake Extreme phenotypic features among species within groups make interpretation of relationships difficult Similar forms with similar mouth structures, feeding behavior and ecological niche grow in different lakes; are they related? Or parallel products of adaptive radiation?

13 Evolution in African Cichlids

14 Evolution in African CichlidsmtDNA phylogeny reveals that cichlid species in different African lakes with equivalent body form and mouth-feeding structures are NOT sister species  rampant parallelism phenotypically and ecologically divergent species typically are sisters extensive divergence in relatives Reinthal & Meyer (1997)

15 Evolution in African CichlidsEvolution in African cichlid fishes (cont.) Ecologically equivalent species in different lakes occupy similar microhabitats, eat same food items  strong selection for similar phenotypes Suggestion of sympatric speciation within individual lakes, accompanied by adaptive radiation based on mouthparts for feeding  reinforcement by competitive exclusion?

16 Diversification in Brocchiniae.g., “pitcher plants” (Brocchinia) on Venezuelan tepuis About 20 species on tall, nutrient-poor (often boggy) sandstone mesas (tepuis) jutting up out of the Venezuelan lowland rainforest Several growth habits and feeding strategies--"tank" habit and carnivory, epiphytes, tree forms, ant-plants Givnish et al. (1997)

17 Diversification in Brocchinia

18 Diversification in Brocchinia“pitcher plants” (Brocchinia) on Venezuelan tepuis (cont.) Morphological and anatomical traits related intimately to growth form and nutrition; tank habit found only at higher elevations Divergent growth forms and feeding strategies obscure the relationships  chloroplast DNA phylogeny used to interpret morphological and ecological evolution Two sister lineages occur primarily on tepuis in different geographic areas

19 Diversification in Brocchinia“pitcher plants” (Brocchinia) on Venezuelan tepuis (cont.)—parallelism of carnivorous traits Givnish et al. (1997)

20 Diversification in Brocchiniastepwise evolution of traits for carnivorous habit Givnish et al. (1997)

21 Evolution in Hawaiian ViolaNine taxa, seven species distributed over most islands Species occupy several different habitats across five islands dry forest dry cliff mesic streambank swamp (cloud) forest open bog Species growing in same habitat on different islands are almost identical morphologically, anatomically

22 Evolution in Hawaiian ViolaHawaiian Islands Price, J. P. a. W. W. L. (2004).

23 Evolution in Hawaiian ViolaPhylogenetic tree of Internal Transcribed Spacer (nrDNA) shows that Hawaiian taxa highly derived (i.e., advanced) in the genus Nearest sister is an Arctic tundra bog violet, Viola langsdorffii, NOT tropical species Ballard & Sytsma (2000)

24 Evolution in Hawaiian ViolaRange of Viola langsdorffii Arctic-breeding birds probably dispersed seeds to Hawaii ca. 75 bird species breed in Arctic, overwinter in central or south Pacific some (e.g., golden plover) arrive in Hawaii by the millions, feed in areas near tundra bogs before migration Ballard & Sytsma (2000)

25 Bog (reclining herb or shrub)Evolution in Hawaiian Viola Bog (reclining herb or shrub) Dry Forest (treelet) Swamp forest (shrub) V. maviensis (Maui, Molokai, Hawaii) V. wailenalenae (Kauai) V. kauaensis (Kauai, Oahu) V. tracheliifolia (Kauai, Oahu, Maui, Molokai) V. robusta (Molokai)

26 Prevailing Trade WindsEvolution in Hawaiian Viola Bog Swamp Forest Dry Forest Very Wet (Bog) Prevailing Trade Winds Wet (Swamp Forest) Dry (Dry Forest) Havran (unpublished data)

27 Evolution in Hawaiian ViolaPhylogenetic tree of ITS sequences, and mapping of islands and habitats onto it: Modest radiation from Arctic tundra bog ancestor Colonization first on Kauai, subsequent diversification and dispersal eastward Parallel evolution in growth form, leaf morphology, leaf anatomy Morphologically “analogous” species on different islands not close relatives

28 Phylogenetic Tree Showing Leaf Traits of Hawaiian ViolaEvolution in Hawaiian Viola Phylogenetic Tree Showing Leaf Traits of Hawaiian Viola

29 Comparative Ecological Studies of “Evolutionary Replicates” Across IslandsReplicate sublineages studied intensively on two different islands, Kaui and Molokai Replicates include: -1 dry forest species (V. tracheliifolia) across islands -2 swamp forest species (V. robusta or V. waialenalenae) -2 bog species (V. kauaensis or V. maviensis) 29

30 Evolution in Hawaiian ViolaEcological research Microhabitat parameters Soil Climate Light Availability Physiological Traits Leaf Anatomy Photosynthetic Physiology Leaf Water Potential Reproductive Biology Breeding Systems Isolation Mechanisms Ethological Temporal V. tracheliifolia Dry Forest V. robusta Swamp Forest V. wailenalenae V. maviensis Bog V. kauaensis Molokai Kauai Havran (unpublished data)

31 V. waialenalenae V. kauaensis

32 Evolution in Hawaiian ViolaExamined % canopy openness, soil moisture, pH, N, C & several micronutrients in populations of 4 spp. Soil moisture & related traits (e.g., C) differentiate spp. N & pH also important, Ca not very important (distinguish bog species) Light etc. contribute little WATER IS KEY! Havran (unpublished data)

33 Evolution in Hawaiian ViolaClimate - Humidity Kauai Molokai Havran (unpublished data)

34 Evolution in Hawaiian ViolaSoil Water Kauai Molokai Bog Swamp Dry Forest Havran (unpublished data)

35 Photosynthetic Efficiency in V. robusta and V. maviensisEvolution in Hawaiian Viola Photosynthetic Efficiency in V. robusta and V. maviensis Swamp forest violet outperforms bog violet at all light levels!? Havran (unpublished data)

36 Leaf Anatomy - Bog VioletsEvolution in Hawaiian Viola Leaf Anatomy - Bog Violets V. maviensis Thick upper and lower epidermis Palisade cells 1 layer thick V. kauaensis Havran (unpublished data)

37 Leaf Anatomy - Swamp VioletsEvolution in Hawaiian Viola Leaf Anatomy - Swamp Violets Thick upper epidermis, thin lower epidermis Palisade cells 2 layers thick Druses present V. robusta V. wailenalenae Havran (unpublished data)

38 Evolution in Hawaiian ViolaMorphologically and anatomically similar species on different islands are not phylogenetic “sister” species Morphologically and anatomically similar species on different islands occupy similar ecological niches soil moisture mainly drives local species distributions in different habitats; anatomy linked to habitats Surprisingly, Swamp Violet (V. wailenalenae) is more photosynthetically efficient at high light levels than Bog Violet (V. kauaensis), but restriction to lower soil moisture prevents it from invading bog! Leaf anatomy appears linked to habitat  Hawaiian violets = adaptive radiation

39 Review A “radiation” is a relatively rapid burst of speciation, producing multiple species from a recent common ancestor Not all lineage radiations are adaptive; researchers must demonstrate a link between environmental selection (habitat) and phenotypes (morphology) Molecular data are valuable to provide a basis for inferring morphological evolution

40 Review Adaptive radiations common on oceanic islands but probably overlooked on continents Two consequences of AR are common and often concurrent: Non-sister species inhabiting similar ecological zones are phenotypically convergent Sister species in different adjacent habitats are phenotypically divergent

41 Bibliography Ballard, H. E., Jr. and K. J. Sytsma Evolution and biogeography of the woody Hawaiian violets (Viola, Violaceae): Arctic origins, herbaceous ancestry, and bird dispersal. Evolution 54: Givnish, T. J. and K. J. Sytsma (eds.) Molecular evolution and adaptive radiation. Cambridge University Press, Cambridge, United Kingdom. 621 pp. Givnish, T. J., K. J. Sytsma, J. F. Smith, W. J. Hahn, D. H. Benzing, and E. M. Burkhardt Molecular evolution and adaptive radiation in Brocchinia (Bromeliaceae: Pitcairnioideae) atop tepuis of the Guayana shield. In: Givnish, T. J. and K. J. Sytsma (eds.), Molecular evolution and adaptive radiation. Cambridge University Press, Cambridge, United Kingdom. pp Niklas, K. J The evolutionary biology of plants. University of Chicago Press, Chicago, Illinois. 449 pp.

42 Bibliography Nitecki, M. H. (ed.) Evolutionary innovations. University of Chicago Press, Chicago, Illinois. 304 pp. Reinthal, P. N. and A. Meyer Molecular phylogenetic tests of speciation models in Lake Malawi cichlid fishes. In: Givnish, T. J. and K. J. Sytsma (eds.), Molecular evolution and adaptive radiation. Cambridge University Press, Cambridge, United Kingdom. pp Schluter, D. and J. D. McPhail Character displacement and replicate adaptive radiation. Trends in Ecology and Evolution 8: