RATES OF DIVERSIFICATION

BACKGROUND Rapid rate of diversification often follows the adaptive radiation + (sexual) selection New niches Mutation New species Adaptive radiation

Examples of adaptive radiation: Galapagos Island finches Tertiary radiation of birds and mammals Cichlid fishes in the African great lakes Galapagos finches Nimbochromis venustus Archaeopteryx

RATE OF DIVERSIFICATION How does the rate of diversification vary through space and time? How does the rate of diversification vary across taxonomic groups and region? What methods do they use to assess the rate of diversification? What could be the future challenges of the methods used in species rate of diversification?

Ecological opportunity Ecological opportunity is a primary factor regulating the tempo of diversification (Schluter 2000; Gavrilets & Vose 2005) Greater ecological opportunity increases the likelihood of lineage divergence saturation of niche space Ecological opportunity (clade acquires species) Rate of diversification

Example: The role of geography and ecological opportunity in the diversification of day geckos (Phelsuma) (Harmon et al. 2008) Phelsuma madagascariensis

Hypothesis that Harmon et al. (2008) tested: Ecological opportunity: rate of speciation and morphological evolution will be elevated following colonization of islands unoccupied by competitor species (Baldwin & Sanderson 1998) Speciation rate is positively correlated with island area (Losos & Schluter 2000) (fig from Losos & Schluter 2000)

Method: ● Maximum Likelihood approach Calculate diversification rate under a number of extinction scenarios (Magallón & Sanderson 2001) Diversification rate ( ϒ -μ) = speciation rate ( ϒ ) - extinction rate (μ) Extinction scenario (ε) = turnover = μ/ ϒ ● Test for slowing through time in diversification rate (Pybus & Harvey 2000)

Rate of species accumulation have slowed through time on Madagascar. Rates of morphological evolution are higher on both the Mascarene and Seychelles archipelagos compared to rate on Madagascar Ecological opportunity is an important factor in diversification of day gecko species (Harmon et al. 2008)

Issues with their model (Harmon et al. 2008) Maximum Likelihood under the null hypothesis of a constant pure-birth process ~ speciation and extinction rates are constant through time. (Stadler 2011) New ML approach The birth–death-shift process, where the speciation and extinction rates can change through time.

Estimating the maximum-likelihood speciation and extinction rates together with the shift times Case of the mammalians (Stadler 2011) ~ 33 mya

(Uyeda et al. 2011) Divergence in body size between related species versus the divergence time Crazy amount of data: Rate of evolutionary change Divergence time Fossil data change through time Methods: Multiple-burst model (“Blunderbuss” model) =Models involving Brownian motion Random variation of the values of the traits around the mean

Want evolutionary change?? Wait a million years !!! (Uyeda et al. 2011)

RATE OF DIVERSIFICATION How does the rate of diversification vary through space and time? How does the rate of diversification vary across taxonomic groups and region? What methods do they use to assess the rate of diversification? What could be the future challenges of the methods used in species rate of diversification?

Ecological opportunity is a primary factor regulating the tempo of diversification (Schluter 2000) Shift to a new habitat would increase the rate of diversification Involves geography, location, areas, range : Important role of space Paleogeography and paleoclimate

(Hou et al. 2011) Habitat shift from saline to fresh water Gammarus lacustrisGammarus balcanus

Hypothesis: Shift to a new habitat frees species from the competition with closely related species and would increase the rate of diversification followed by adaptive radiations Methods: Phylogenetic inference: to estimate the divergence times of its major lineages to determine when the shift from saline to freshwater occurred. Biogeographic analysis (Likelihood and Parsimony methods) to explore where Gammarus first colonized freshwater habitats Diversification analysis to assess the temporal diversification mode associated with the habitat shift (Hou et al. 2011)

Results: Phylogenetic inference identifies an Eocene habitat shift from saline to freshwater Biogeographic analysis indicates two major range shifts (Hou et al. 2011)

Results: Diversification modes associated with habitat shift

Habitat shift from saline to freshwater + Increase of land mass Available bodies of freshwater Rapid radiation of freshwater species

Habitat shift from saline to freshwater + Increase of land mass Available bodies of freshwater Rapid radiation of freshwater species

RATE OF DIVERSIFICATION How does the rate of diversification vary through space and time? Geography and space Biological history Climate

RATE OF DIVERSIFICATION How does the rate of diversification vary through space and time? Geography and space Biological history Climate Extrinsic causes due to new environmental circumstances

RATE OF DIVERSIFICATION How does the rate of diversification vary through space and time? Geography and space Biological history Climate Extrinsic causes due to new environmental circumstances Radiations may occur due to intrinsic characters of organisms ➔ the key innovation

How does the rate of diversification vary through space and time? Rapid radiation due to a key innovation Aquilegia (Ranunculaceae) (Hodges 1997) Methods: Phylogenetic analyses - test for monophyly – a basic assumption of adaptive radiation - identification of sister taxa – by definition of equal age - evolution of proposed key innovation – floral spurs

Rapid radiation due to a key innovation in Columbines (Ranunculaceae: Aquilegia) (Hodges 1997)

Rapid radiation of Aquilegia: via key innovation or via invasion of new habitat?

Role of space Aquilegia and its close relatives Isopyrum do not occupy a substantially different geographic range. It does not appear that Aquilegia has dispersed into a new habitat that its close relatives were unable to invade.

Spur as key innovation Underlying assumption of most species concepts: the necessity for reproductive isolation Characters that can promote reproductive isolation may increase speciation rate and thus diversification Taxa with spurs can become specialized on different pollinator types which increases reproductive isolation and possibly speciation (Hodges 1997)

How to know if there has actually been a change in diversification rate between sister taxa? Assessing weather branching rate increases with origin of traits Change in diversification should be associated with the branch where the key innovation evolved Comparison of the diversification rate of the sister group lacking the key innovation and the lineages that possess the proposed key innovation (Sanderson & Donoghue 1994)

Methods: Method based on ML approach Null model as test for changes in diversification rate Null model (Yule pure birth) assumes a (unknown) constant lineage birth rate for each branch on the tree (1) Calculate the likelihood of observing N species in a clade after an interval time d (2) Markov property of (1) permit multiplication of (2) taking into account different rate parameters in different branches Different ML models with various number of rate parameters (Sanderson & Donoghue 1994)

P values > 0.95 model rejected rejected accepted

Rapid rate of diversification often follows the adaptive radiation Selection New niches Mutation New species Adaptive radiation

Rapid rate of diversification often follows the adaptive radiation Selection New niches Mutation New species Adaptive radiation

(Gavrilets & Vose 2005) Genetically based habitat choice models of large-scale evolutionary diversification Preference for new niche New ecological niche environmental factors Simultaneous Genetically controlled Each individual has different neutral loci subject to mutation Probability of extinction is assigned per generation (turn over of ecological niches)

(Gavrilets & Vose 2005)

➔ Larger areas allow for more intensive diversification (area effect) new locally advantageous genes may become better protected by distance from the diluting effect of locally deleterious genes, which otherwise can easily prevent adaptation to a new niche. Anolis lividus Anolis gorgonae Anolis nitens (Gavrilets & Vose 2005)

➔ Increasing the number of loci underlying the traits decreases diversification a larger number of loci implies weaker selection per each individual locus and a stronger overall effect of recombination in destroying co-adapted gene complexes. Anolis lividus Anolis gorgonae Anolis nitens (Gavrilets & Vose 2005)

The level of divergence in neutral microsatellite loci between populations from different species is comparable to that between populations of the same species. blue butterfly species Lycaeides melissaLycaeides idas

➔ The number of species peaks early in the radiation speciation events occur soon after colonization of a new environment so the genetic constraints are less strict than later on. Tetragnatha sp. (Gavrilets & Vose 2005)

Summary and conclusion: Adaptive radiation is defined as the evolution of ecological and phenotypic diversity within a rapidly multiplying lineage. When it occurs, adaptive radiation typically follows the colonization of a new environment or the establishment of a “key innovation” which opens new ecological niches and/or new paths for evolution. The increasing availability of molecular phylogenies and associated divergence times has spurred the development of new methods to estimate rates of speciation and extinction from phylogenetic data of extant species and to detect changes in diversification rates through time and across lineages.

QUESTIONS: Phylogeny is indispensable in understanding the diversification rate, how about its reliability? What would be the effect of the interplay between adaptive radiation and extinction on the tempo and timing of lineage diversification? (Antonelli & Sanmartin 2011) Recent radiation or signature of extinction??