BIO232: Macroecology , Niche evolution, and Climate Change

1. BIO232: Macroecology, Niche evolution, and Climate Change Ecological Niches and Evolution Elena Conti Institute of Systematic Botany and Botanic Garden University of Zurich

2. 1. Background 2. Ecology & evolution 3. Niche conservatism vs. evolution 4. Integrative biogeography Ecological Niche and Evolution: OUTLINE • PART 1 – DAY 1 • Background • Questions • Phylogenies: how to read them • Speciation: species concepts, reproductive isolation, geographic context • Integrating ecology and evolution: Questions and examples • Limonium • Haplophyllum • Primula sect. Primula • Primula sect. Aleuritia • PART 2 – DAY 2 • Primulasect.Primula ecological niches and polyploid speciation • Hindcasting: Pleistocene glacial cycles, Saxifragaflorulenta • Forecasting: species responses to climate change • Niche conservatism vs. niche evolution • controversy • examples • theoretical considerations • problems • Integrating ecological and historical biogeography: example

3. 1. Background 2. Ecology & evolution 3. Niche conservatism vs. evolution 4. Integrative biogeography QUESTIONS • What is the role of ecological niches in evolution? • How can we use niche modeling and other macro-ecological tools to ask evolutionary questions? (continuous vs. discrete definitions of trait variation within a group of related species: see Phylogeny Lab with Bianca Saladini and NICK ZIMMERMANN) • What kinds of questions can we ask using ecological niche models that will elucidate evolutionary patterns and processes? • SOME USEFUL KEYWORDS, CONCEPTS • Macro-evolution and micro-evolution: evolution at two different temporal (and, often, spatial) scales • Patterns and process in evolution: micro-evolutionary processes (e.g., population differentiation, speciation, etc…) produce evolutionary outcomes that can be described as specific phylogenetic patterns (i.e., phylogenetic topologies)

4. 1. Background 2. Ecology & evolution 3. Niche conservatism vs. evolution 4. Integrative biogeography Let’s start from the Macro-evolutionary level: a Phylogeny A B C D E F x G y z This is a phylogenetic tree: it represents evolutionary relationships among a set of 7 species How to read this tree (see Baumand Smith, 2012. Tree Thinking) • Are all species extant (i.e., living) or not? • What are the specific statements that one can make on the relationships among these 7 species, based on this tree? • What does the tree imply concerning the internal nodes of the tree x, y, and z? • Why are the internal nodes represented as fuzzy clouds?

5. 1. Background 2. Ecology & evolution 3. Niche conservatism vs. evolution 4. Integrative biogeography A B C D E F x G y z Let’s imagine that the seven species are characterized by a variety of ecological or habitat preferences; we could also call them “ecological niches” and they could be defined as discrete or continuous variables or as niche models • Would you expect ecological preferences to be more similar between closely related species or not? Why? • Would your expectations change if I told you additional information about species distributional ranges? • Case 1: sister species have overlapping distributional ranges • Case 2: sister species have mutually exclusive distributional ranges • Case 3: some sister species have overlapping ranges, some sister species have mutually exclusive ranges  Niche conservatism vs. niche evolution

6. 1. Background 2. Ecology & evolution 3. Niche conservatism vs. evolution 4. Integrative biogeography To better understand the topic of niche conservatism vs. niche evolution, we need to think a bit harder about what goes on at the nodes of a phylogeny. A B C D E F x G y z What happens at the nodes of a phylogeny? Cladogenesis=species divergence=speciation Speciation: boundary between MICROEVOLUTION (genetic changes within species anagenesis) and MACROEVOLUTION (evolution of higher taxa cladogenesis) Speciation: where pattern and process meet • How are species formed? • What are the processes, causes, drivers of species divergence?

7. 1. Background 2. Ecology & evolution 3. Niche conservatism vs. evolution 4. Integrative biogeography SPECIES CONCEPTS (from Futuyma 2005) Using the BSC, we can then define speciation as: “The evolution of genetically distinct populations, maintained by reproductive isolation in the case of sexual taxa” (Bolnick and Fitzpatrick, 2007)

8. 1. Background 2. Ecology & evolution 3. Niche conservatism vs. evolution 4. Integrative biogeography SPECIATION: • Intrinsic vs. extrinsic barriers to gene flow between species •  types of reproductive isolation • Geographic context of species divergence

9. 1. Background 2. Ecology & evolution 3. Niche conservatism vs. evolution 4. Integrative biogeography PREMATING ISOLATING MECHANISMS: Features that impede transfer of gametes to members of other species Role of ecological differences in reproductive isolation: Species have propensities to occupy different habitats when they occur in the same general area. Differential adaptation, etc… From Coyne and Orr, 2004

10. 1. Background 2. Ecology & evolution 3. Niche conservatism vs. evolution 4. Integrative biogeography POST-MATING,PRE-ZYGOTIC MECHANISMS: Male gametes are transferred, but fertilization is prevented POST-ZYGOTIC MECHANISMS: Hybrid zygotes are formed, but have reduced fitness Role of ecological differences in reproductive isolation: Hybrids less fit for available habitat than either parental species. Habitat selects against hybrids, blocking inter-specific gene flow. From Coyne and Orr, 2004

11. 1. Background 2. Ecology & evolution 3. Niche conservatism vs. evolution 4. Integrative biogeography Role of ecological differences in speciation: Immigrant inviability: Natural selection against immigrants into new environments can reduce interbreeding between populations, acting as a barrier to gene flow (Nosil, P. 2012. Ecological Speciation) Role of extrinsic barriers in speciation: Physical geographic features reduce or eliminate gene flow between populations  allopatric speciation

12. 1. Background 2. Ecology & evolution 3. Niche conservatism vs. evolution 4. Integrative biogeography • Geographic context of Speciation • Geographic relation of populations/species to each other • Allopatric (vicariance & peripatric) • Parapatric • Sympatric • Genetic and selective bases Futuyma, 2005

13. 1. Background 2. Ecology & evolution 3. Niche conservatism vs. evolution 4. Integrative biogeography Geographic context of speciation: continuum • Lowest gene flow • Low selection may still allow for species divergence (genetic drift) • Panmixis • High selection necessary for species divergence Futuyma, 2005

14. 1. Background 2. Ecology & evolution 3. Niche conservatism vs. evolution 4. Integrative biogeography • Allopatric speciation: vicariant and peripatric • Evolution of genetic reproductive barriers between geographically separated populations (by drift, neutral processes). • Physical barriers: mountain, river, ocean, unfavorable habitat Defined by drastic reduction in the movement of gametes or individuals, NOT by geographic distance per se. VICARIANT SPECIATION: A previously continuous population is divided by a barrier • Allopatrically formed species can come into contact againSECONDARY CONTACT: • If their reproductive barriers are complete or near complete, they will not hybridize. • If reproductive isolation is incomplete, they may form hybrid zones or new hybrid species • Contemporary species that occur in sympatry may have formed allopatrically

15. 1. Background 2. Ecology & evolution 3. Niche conservatism vs. evolution 4. Integrative biogeography Peripatric speciation Also known as “founder effect” speciation (Mayr 1954, 1982) Isolated populations with restricted distributions, in locations peripheral to the distribution of a probable “parent” species, are often highly divergent, both phenotypically and genetically. If a new population is cut off from gene flow with the “source” population, genetic changes can accumulate fast by genetic drift. The change in genetic interactions (epistasis) could accidentally affect the loci that control reproductive isolation (BDM model: Bateson-Dobzhansky-Mueller genetic incompatibilites)

16. 1. Background 2. Ecology & evolution 3. Niche conservatism vs. evolution 4. Integrative biogeography Parapatric speciation Divergent selection, even with a small environmental discontinuity, may be sufficient to counteract gene flow and result in reproductive isolation. This geographic context of speciation seems to be especially relevant to ecological speciation, hence to the importance of the ecological niche in the speciation process.

17. 1. Background 2. Ecology & evolution 3. Niche conservatism vs. evolution 4. Integrative biogeography Problem with sympatric speciation: How to reduce the frequency of intermediate genotypes that allow for gene exchange between the two incipient species, thus preventing full species divergence. Mayr (1904-2005): most vigorous opponent of sympatric speciation Sympatric speciation Ancestral population: panmixis • Models of sympatric speciation require: • Divergent (or disruptive, or diversifying) selection: • Homozygous phenotypes are optimally adapted to certain resources; heterozygote phenotypes less so, so they have lower fitness • Divergent adaptation may be based on one or several loci • Nonrandom (i.e., assortative) mating reduces the frequency of unfit heterozygous offspring • The incipient species thus differ at several loci governing adaptation and mating (i.e., reproductive isolation) • BUT: recombination would break up these co-adapted gene packages, unless the relevant genes were very close to each other (i.e., in linkage disequilibrium) Genetic differences result in reproductive isolation between two groups of individuals

18. 1. Background 2. Ecology & evolution 3. Niche conservatism vs. evolution 4. Integrative biogeography The allopatry to sympatry spectrum (Fig. 6.2. from Nosil, 2012; after Mallet, 2009)

19. 1. Background 2. Ecology & evolution 3. Niche conservatism vs. evolution 4. Integrative biogeography The allopatry to sympatry spectrum • Let’s stop for a moment and think about the geographic context of speciation: • How do concepts of allopatry, parapatry, and sympatry relate to concepts of geographic ranges and how they relate to each other?

20. 1. Background 2. Ecology & evolution 3. Niche conservatism vs. evolution 4. Integrative biogeography The continuous nature of speciation Ecological perspectives on speciation: • Are the ecological niches of sister species different or similar? • Can ENMs help us: To compare the ecological preferences of sister species? To study speciation? • What are the variables that affect the answer to this question? • See: Warren DL. 2012.In defense of “niche modeling”TREE 27:497, for cautions on ENMs vs. SDMs • Can you think of examples of steep ecological gradients? Nosil et al. 2009. Ecological explanations for (incomplete) speciation. Trends in Ecology and Evolution 24:145

21. BREAK

22. - Unexploitedhabitats open up possibilitiesforecologicaldiversification - Radiations and highendemicitylevels 1. Background 2. Ecology & evolution 3. Niche conservatism vs. evolution 4. Integrative biogeography How to think about integrating ecological and evolutionary analyses: - Which questions can we ask? Example 1. Speciation in oceanic islands Oceanicislands - Emerge fromthe sea empty of life

23. How to think about integrating ecological and evolutionary analyses: - Which questions can we ask? Intra- vs. inter-islandspeciation Twopotentialmodelsforspeciationonoceanicislands: 1.- Intra-islandspeciation(sympatricorparapatric): potentialtocolonize new habitats. Adaptation to new niches Coastal dunes Coastal cliffs Low elevational belt Intermediate elevational belt Mountain tops

24. How to think about integrating ecological and evolutionary analyses: - Which questions can we ask? Intra- vs. inter-islandspeciation Two potential models for species evolution on oceanic islands: 2.- Inter-islandspeciation (“allopatric”): stableecologicalpreferences. Niche conservatism

25. How to think about integrating ecological and evolutionary analyses: - Which questions can we ask? Intra- vs. inter-islandspeciation: phylogeneticexpectations Do sisterspeciesoccuronthesameisland? Do theyoccupydifferenthabitats? Sp. 1 Island A Habitat Y Sp. 2 Island A Habitat Z Sp. 3 Island B Habitat Y If yes intra-island speciation, driven by ecological differentiation Sp. 4 Island B Habitat Z Do sisterspeciesoccurondifferentislands? Do theyoccupythesamehabitat? Sp. 1 Island A Habitat Y Sp. 2 Island B Habitat Y Sp. 3 Island A Habitat Z If yes inter-island speciation, driven by physical geographic barriers Sp. 4 Island B Habitat Z

26. How to think about integrating ecological and evolutionary analyses: - Which questions can we ask? Intra- vs. inter-islandspeciation: phylogeneticexpectations Thepicture can be more complex! Sp. 1 Island A Habitat X Sp. 2 Island B Habitat X Sp. 1 Island A Habitat Y Sp. 1 occursononeisland and has broaderenvironmentaltolerancesSp. 2 occurson a differentisland and has environmentaltolerancesthat are a subset of those of sp. 1:  paraphyly! Sp. 2 derivedfromwithinsp. 1; populations of sp. 1 in thesamehabitat of sp. 2 are more closelyrelatedtosp. 2 (eventhoughthey are ondifferentislands), thanthey are tootherpopulations of thesamespeciesthatoccur in differenthabitatsonthesameisland Sp. 1 Island A Habitat Z

27. How to think about integrating ecological and evolutionary analyses: - Which questions can we ask? CanaryIslands • Complextopography and widediversity of habitats: * Arid coastal * Semi-dry transition belt * Cloud belt area Lanzarote * High semi-dry La Palma * High-mountain arid Tenerife La Gomera Fuerteventura Gran Canaria El Hierro

28. * Habitats Cliffs Salt-rich lagoons Rocky shores Coastal Inland Gypsum soils Sandy shores Deserts Marshes * Main ecological factors: - Salinity - Water availability How to think about integrating ecological and evolutionary analyses: - Which questions can we ask? Genus Limonium * About 400 species worldwide.

29. L. arborescens (LP, T) • L. benmageci(GC) • L. bourgeaui(L, F) • L. brassicifoliumsusbp. • L. brassicifoliumsusbp. • L. fruticans(T) • L. imbricatum(T, LP) • L. macrophyllum(T) • L. perezii(T) • L. preauxii(GC) • L. puberulum(L) • L. redivivum(LG) • L. relicticum(LG) • L. spectabile(T) • L. sventenii(GC) • L. vigaroense(GC) brassicifolium(LG) macropterum(EH) How to think about integrating ecological and evolutionary analyses: - Which questions can we ask? Limonium in theCanaryIslands • Nobilesgroup: 16 taxa • 13 endemicto 1 island • 3 endemicto 2 islands Lanzarote 3 11 La Palma 1 7 1 6 7 8 9 14 Tenerife 3 Fuerteventura La Gomera 4 12 13 Gran Canaria 2 10 15 16 El Hierro 5

30. L. bourgeaui (L) L. preauxii (C) L. puberulum (L) L. sventenii (C) L. macrophyllum (T) L. fruticans (T) L. redivivum (G) L. arborescens (T) L. imbricatum (T) How to think about integrating ecological and evolutionary analyses: - Which questions can we ask? Limonium: Nobilesgroupin theCanaryIslands

31. trnL-F, rbcL (Lledó et al. 2011) Limonium phylogenies Morphological characters (Karis 2004) Putativelymonophyletic (5 out of 16 spp. in Nobiles) Sect. Pteroclados, Subs. Nobiles Putativelymonophyletic (13 out of 16 spp. sampled) 1 2 3 4 5 1 3 4 5 2

32. How to think about integrating ecological and evolutionary analyses: - Which questions can we ask? Limonium (Nobilesgroup) in theCanaryIslands: morphologicalphylogeny (Karis 2004) ISLAND+no. of KNOWN POPS HABITAT TYPES L. preauxii L. macrophyllum L. spectabile L. imbricatum L. macropterum L. brassicifolium L. redivivum L. puberulum L. bourgeaui L. perezii L. sventenii L. fruticans L. arborescens L. benmageci L. vigaroense L. relicticum C12 T 5 T 3 T 4, P3 H2 G2 G3 L1 L1, F1 T 1 C4 T 1 T 5, P1 C1 C3 G1 I-Xe C-3 C-0, C-1, C-2 C-0, C-1, C-2 C-2, C-3 C-2, C-3 I-Hu C-0, C-1, C-2, C-3 C-2, C-3 C-3 C-3, I-Hu C-1, C-2 C-2, C-3 C-2 I-Hu C-3 ISLANDS LLanzarote FFuerteventura CGran Canaria T Tenerife GLa Gomera PLa Palma HEl Hierro Allopatric sister species on different islands occupy same habitat: niche conservatism? Two species on same islands, habitat of one species subset of habitat of the other species: niche specialization? HABITATS C-0 Rocky shores C-1 Coastal cliffs < 100m C-2 Coastal cliffs 100-400m C-3 Coastal cliffs > 400m I-Xe Inland xeric slopes 200-900m I-Hu Inland humid cliffs > 600m Different islands, different habitats: niche divergence after allopatric speciation? ?

33. How to think about integrating ecological and evolutionary analyses: - Which questions can we ask? Example 2. Haplophyllum(Rutaceae) in the Irano-Turanian region H.bucharicum H.villosum Mountains H.rechingeri H. virgatum Desert Roadsides Sarah Manafzadeh Ph.D. student Agricultaral lands Rocky slopes H.viridulum H.bungei Stony slopes H.dasygynum H.robustum H.furfuraceum H.acutifolium

34. How to think about integrating ecological and evolutionary analyses: - Which questions can we ask? Example 2. Haplophyllum(Rutaceae) in the Irano-Turanian region

35. Example 2. Haplophyllum(Rutaceae) in the Irano-Turanian region

36. How to think about integrating ecological and evolutionary analyses: - Which questions can we ask? Example 3. Primula sect. Primula Primula elatior less sunny and more dampish site Primula veris Sunnier, driersite Dr. Barbara Keller, post-doc Jonelisweid (Simmental, BE), Switzerland

37. Primula veris Less open anddrier sites Primula vulgaris More open and dampish sites Sonzier (Montreux, VD)

38. Primula elatior • Meadows, woods, hedges that are moist or seasonally waterlogged • Poorly developed drought tolerance • Colline-subalpine(-alpine) (CH) Primula vulgaris • Open woods, orchard meadows, hedges • Colline-montane (CH) Primula veris • Typical species of (nutrient-poor) calcareous grasslands • Intolerant of waterlogged soils • Only rarely found in shaded habitat • Colline-subalpine (CH)

39. P. elatior How to think about integrating ecological and evolutionary analyses: - Which questions can we ask? Example 3. Primula sect. Primula P. elatior P. vulgaris P. veris P. vulgaris P. elatior x P. vulgaris P. veris

40. Primulafarinosa: Romania, peatbog, 526 m, How to think about integrating ecological and evolutionary analyses: - Which questions can we ask? Example 4:Primula sect. Aleuritia Primulafarinosa: Bulgaria, alpine streams of melting snow in Pirin Mts. Spyros TheodoridisPh.D. student Primulahalleri: Bulgaria, Pirin Mts. 2146 m. Soil drier, temp. excursions more extreme. Primulahalleri: Romania, a few Km away from previous site and higher; steep slope on Bucegi Mt., 2061 m. Soil drier, temp. excursions more extreme.

41. How to think about integrating ecological and evolutionary analyses: - Which questions can we ask? Distribution of European Aleuritia species Example 4:Primula sect. Aleuritia • The distributional ranges of P. farinosaand P. hallerioverlap in the Alps and in the Eastern European mountain ranges: • Species divergence may be related to ecological differentiation • Are they sister species? • Additional factor: polyploidization

42. How to think about integrating ecological and evolutionary analyses: - Which questions can we ask? • Did you notice any major differences concerning the ecological variation of the four case studies above? • What is the geographic context of speciation? Do sister species occur in sympatry, parapatry, or allopatry? Why is it important to consider the geographic context of speciation, when studying the role of ecology in speciation? • Given a group of related species that show variation of habitat preferences, we can ask: • Is speciation (diversification) in the genus driven by ecological differentiation or by geographic separation (allopatry)? • Are the ecological preferences of closely related species more similar to each other than expected by random processes? • (See summary of analyses to test for this in Crisp and Cook, 2012. Phylogenetic niche conservatism: what are the underlying evolutionary and ecological causes? New Phytologist, 196:681-694)

43. How to think about integrating ecological and evolutionary analyses: - Which questions can we ask? • Which kinds of information do we need to answer these questions? • Set of variables that describe the habitat preferences of the species (either as discrete or continuous variables or as niche models) • Phylogenetic tree to determine patterns of relatedness • General distributional ranges of species to determine the geographic context of speciation • Ideally, link between ecological preferences and functional traits, and speciation process (most difficult, usually requires experiments under controlled conditions, reciprocal transplants, etc.)