Macroevolutionary Processes— Radiations

1. Macroevolutionary Processes— Radiations

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

3. Concepts Involving Radiations • Definition 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 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

5. 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

6. 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

7. 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

8. 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

9. Canary Island Land Snails (Theba) Africa Photos: GoogleEarth; Greve et al. 2012. PLOS One 7(4): e34339

10. Canary Island Land Snails (Theba) T. impugnata T. grassetti Photos: Greve et al. 2012. PLOS One 7(4): e34339

11. Canary Island Land Snails (Theba) • Many phenotypically and genetically differentiated land snail species • Phenetic/morphometric analysis revealed only two unusually divergent species • The anomalous species showed no clear association with extreme habitats  no obviously “adaptive” traits corresponding with ecological specialization  NOT an adaptive radiation

12. 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

13. Sexual Radiation • Result of sexual selection toward premating isolation mechanisms • Differentiation is primarily in courtship behaviors, genitalic features, other traits associated with reproduction • Direction of selection does not track environmental factors • e.g., fruit fly (Drosophila) diversification

14. 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

15. 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

16. 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?

17. 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?

18. 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

19. 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

20. 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

21. 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

22. 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

23. 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?

24. Case Studies of Radiation

25. 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)

26. 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?

27. 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)

28. Case Studies of Radiation

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. Case Studies of Radiation

34. 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

35. 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

36. 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

37. 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.

38. 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.