Macroevolutionary Processes— Radiations

1. Macroevolutionary Processes— Radiations

2. Review • plant breeding systems span range from obligately selfing to obligately outcrossing • various strategies have evolved to promote outcrossing; major ones are: • self-incompatibility—chemical control of pollen germination on style • heterostyly—mechanical prevention of pollen deposition by relative displacement of anthers and stigma

3. Review • dioecy—separation of sexes on different plants • each breeding system has different molecular genetic regulation • breeding systems can flip-flop back and forth, even within lineages—evolutionarily labile

4. Concepts Involving Radiations • Definition of “radiation”--relatively rapid diversification of an initial population into several closely related 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

5. Concepts Involving Radiations • Character 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

6. Adaptive Radiation • “The rise of a diversity of ecological roles and attendant adaptations in different species within a lineage" (Givnish and Sytsma) • Recently loosely applied to all bursts of diversification, but attempts made recently to restrict definition—does not necessarily result in a huge increase in species number or require a "key innovation"

7. Adaptive Radiation • Correctly defined examples require convincing demonstrations/inferences: • 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

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

9. Non-adaptive Radiation • Also termed “diffusive evolution” • "Evolution abhors a vacuum—whenever possible, organisms will evolve by chance into and come to occupy all regions in the domain of theoretically possible phenotypes that permit survival and reproductive success" (Niklaus)  speciation without appreciable ecological divergence and evolution of corresponding adaptations • Usually results in single origin of key trait • Usual pattern of geographic or other speciation • Better explains certain traits in putatively adaptive radiations, e.g., arborescence

10. Developmental Radiation • e.g., new body-plan rearrangements in Precambrian, with possible advent of newly arising, divergent sets of homeotic genes controlling different organs/systems • Could be involved at lower level in each adaptive radiation

11. Sexual Radiation • Result of sexual selection toward premating isolation mechanisms • Direction of selection does not track environmental factors • e.g., fruit fly (Drosophila) diversification

12. Coevolutionary Radiation • Intimate 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

13. Interesting Questions • Do phenotypic or ecological similarities reliably reflect phylogenetic relationships in a group produced in a radiation? • What evidence exists to indicate certain species differences are adaptive, fitting them to their divergent evolutionary roles? • What environmental factors may have "driven" diversification of particular phenotypic traits, or syndromes

14. Interesting Questions • Does selection for ecological divergence result in speciation? • What is the level of genetic divergence among species and their populations in a radiation? • How labile are the phenotypic traits and physiological tolerances in species of a radiation?

15. Interesting Questions • What is the relation between local geography, ecology and speciation in a radiation? • Have similar-looking radiations occurred in very distantly related groups, leaving behind some fundamental patterns of diversification and convergence? • Are radiations more likely to proceed in certain places or under certain circumstances?

16. Evolutionary Radiations • Virtually all studies explicitly concerned with evolutionary radiation identified with "adaptive radiation", many attempt to identify key innovations • Many strictly phylogenetic/molecular systematic studies could be used for inference of diffusive evolution with small amount of additional information

17. Evolutionary Radiations • 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

18. Evolutionary Radiations • 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

19. Molecular Data in Radiations • Phenotypic features in any type of radiation may be prone to extensive parallelism where more distantly related (=non-sister) taxa grow in same habitat and have evolved similar morphologies • Conversely, closely related taxa may have diverged dramatically in morphology and ecology and do not resemble each other • "Weird" or extreme phenotypic traits in certain organisms sometimes confound interpretation of relationships; e.g., bizarre families like carnivorous plant groups

20. Molecular Data in Radiations • Use 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

21. Case Studies of Radiation • e.g., evolution in African cichlid fishes • Several 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?

22. Pleistocene Lakes in SE Africa

23. African Cichlids from Lakes Malawi & Victoria

24. Case Studies of Radiation • Evolution in African cichlid fishes (cont.) • mtDNA 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)

25. Case Studies of Radiation • Evolution 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?

26. Case Studies of Radiation • e.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)

27. Brocchiniareducta Photos: www.siamexotica.com/Brocchinia.html

28. Tepuis in S Venezuela

29. Case Studies of Radiation • “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

30. Case Studies of Radiation • “pitcher plants” (Brocchinia) on Venezuelan tepuis (cont.)—parallelism of carnivorous traits Givnish et al. (1997)

31. Case Studies of Radiation • “pitcher plants” (Brocchinia) on Venezuelan tepuis (cont.)—stepwise evolution of carnivorous habits Givnish et al. (1997)

32. Case Studies of Radiation • e.g., Hawaiian violets (Viola) • Nine 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

33. Ages of the Hawaiian Islands Kauai = 5.1 my Oahu = 3.7-2.6 my Maui Nui complex = 1.9 my-800,000 y Hawaii = 400,000-180,000 my

34. Topography of Kauai Alakai Swamp/Mt Waialeale (wettest place on earth) High-elevation wet forest, cliffs Waimea Canyon (extremely arid) Low-elevation Moist forest Sandy or rocky Coastal sites

35. Some Viola species on Kauai Viola wailenalenae (shrub, swamp) Viola kauaiensis (herb, open bog) Viola tracheliifolia (treelet, dry forest)

36. Case Studies of Radiation • Hawaiian violets (cont.) • Nuclear gene (ITS) phylogeny used to interpret relationships • Morphologically and ecologically equivalent species on different islands are not sisters • Closest relatives on the same island (= derivatives of local radiation) are phenotypically and ecologically divergent Ballard (unpubl.); Havran et al. (2009)

37. Principal Components Analysis of Leaf Characters Ballard et al. (unpubl.)

38. Leaf Anatomy of Violets on Kauai V.kauaensis—thick UE & LE; tall palisade cells 1 layer thick V.tracheliifolia—thick UE, 1-2 layers, thin LE; short palisade cells, 1-2 layers thick; druses V.wailenalenae—thick UE, thin LE; short palisade cells, 1-2 layers thick; druses Havran (unpubl.)

39. Leaf traits and ecophysiology are linked to habitats Havran et al. (2009)

40. Source Areas for Wintering Hawaiian Songbirds Ballard and Sytsma (2000)

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

42. Review • Adaptive radiations common on oceanic islands but probably overlooked on continents • Two frequent situations in adaptive radiations • Non-sister species inhabiting similar ecological zones are morphologically convergent • Sister species in different habitats are morphologically very different

43. Bibliography • Givnish, T. J. and K. J. Sytsma (eds.). 1997. 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. 1997. 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. 259-311. • Niklas, K. J. 1997. The evolutionary biology of plants. University of Chicago Press, Chicago, Illinois. 449 pp.

44. Bibliography • Nitecki, M. H. (ed.). 1990. Evolutionary innovations. University of Chicago Press, Chicago, Illinois. 304 pp. • Reinthal, P. N. and A. Meyer. 1997. 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. 376-390. • Schluter, D. and J. D. McPhail. 1993. Character displacement and replicate adaptive radiation. Trends in Ecology and Evolution 8:197-200.