Speciation Reversal and Biodiversity Dynamics with Hybridization in Changing Environments

Speciation reversal and biodiversity dynamics with hybridization in changing environments

Ole Seehausen1,2, Gaku Takimoto1, Jukka Jokela1,3 1EAWAG Kastanienbaum Centre of Ecology, Evolution & Biogeochemistry Switzerland 2Institute of Zoology, University of Bern Switzerland PC2 3Institute of Integrative Biology, ETH-Zürich Switzerland

PC1 Hybridization and diversity dynamics

1. the concept of speciation reversal

2. examples

3. the flip side: hybridization as a source of diversity

4. diversity dynamics with hybridization: a simple model

5. conclusions Genetic admixture as a cause of diversity loss: the concept

To the extent that species diversity is made of species that in principle can produce viable and fertile offspring, one way by which species richness can decrease rapidly is by removal of mechanisms that restrict gene flow between the species: This condition is given for a large fraction of species diversity

~5 MY Coyne & Orr 1989; 1997 Examples of species diversity vulnerable to genetic collapse

ttp://www.cof.orst.edu/wolves/miscphotos.php

Oak trees Darwin‘s finches

http://www.wildnatureimages.com/Coyotes.htm wild canids African cichlids

Pacific salmon Genetic admixture as a cause of diversity loss: the concept

Rhymer, J.M., and Simberloff, D. (1996). Extinction by hybridization and introgression. Ann. Rev. Ecol. Syst. 27, 83–109

Ways in which introgressive hybridization rates can be affected by humans:

1. Local habitat modification => loss of adaptive genetic structure through ecological homogenization

2. Regional habitat modification => loss of spatial genetic structure through landscape homogenization

3. Species translocations

4. Habitat fragmentation => small population sizes, unavailability of suitable conspecific mates

All these human impacts are increasing and often act synergistically Genetic admixture as a cause of diversity loss: the concept

Rhymer, J.M., and Simberloff, D. (1996). Extinction by hybridization and introgression. Ann. Rev. Ecol. Syst. 27, 83–109

Ways in which introgressive hybridization rates can be affected by humans:

1. Local habitat modification => loss of adaptive genetic structure through ecological homogenization

2. Regional habitat modification => loss of spatial genetic structure through landscape homogenization

3. Species translocations

4. Habitat fragmentation => small population sizes, unavailability of suitable conspecific mates

All these human impacts are increasing and often they act synergistically Species loss through genetic admixture: examples

Loss of species through genetic admixture after local habitat modification

Taxon environmental change reference Tradescantia subaspera homogenization soil & light environment Anderson & Hubricht 1938 x T. canaliculata Yellow-crowned x Red-fronted exact causes unknown Cade 1983 Parakeet Hyla cinerea x H. gratiosa homogenization of communication env. Lamb & Avise 1986 Iris fulva x I. hexagona homogenization flooding regime Arnold & Bennett 1993

Rhymer, J.M., and Simberloff, D. (1996). Extinction by hybridization and introgression. Ann. Rev. Ecol. Syst. Speciation reversal

If species originated in response to divergent selection, then re-admixture because of a change in the balance between selection and gene flow is conceptually straight forward and is effectively speciation reversal The potential must be widespread if ecological speciation is widespread whereby genetic differentiation is a by-product of divergent adaptation

Seehausen 2006 Current Biology Speciation reversal

Steeply sloping valleys in an adaptive landscape are an effective ecological restriction to gene flow, and many closely related species may have evolved as a by-product of divergent adaptation. Flattening of the adaptive landscape removes ecological restrictions to gene flow and should lead to admixture of species that were maintained by divergent adaptation fitness

phenotypic trait Speciation reversal case 1: sticklebacks

Collapse of species pair precipitated by loss of habitat heterogeneity (habitat structure and water clarity)

Taylor et al. 2006; Gow et al. 2006 Speciation reversal case 2: Lake Victoria cichlids

Pundamilia nyererei and P. pundamilia, a completely sympatric pair of cichlid species endemic to Lake Victoria

65 55 60 68

50km Speciation reversal case 2: Lake Victoria cichlids Genetic and phenotypic distinctiveness is a function of heterogeneity of ambient light environment0.04 1

AFLPs 0.8 0.03 80 60 11 STRs 40 20 0.6 0 123456

0.02 20 0.4

30 10

20 0 10 123456 0.2 0 123456

0.01 Proportion of intermediates 0 Makobe Anchor Nyegezi Kissenda Marumbi Matumbi Igombe Ruti Hippo Python Shadi Luanso genetic differentiation (Fst)

0 500 0 50 100 150 200 250 400 water clarity (cm) 300 Phenotypic and neutral genetic differentiation of sympatric species as a 200 function of water clarity (the latter is very strongly positively correlated with the band 100 width of the ambient aquatic light spectrum) 0 Makobe Anchor Nyegezi Kissenda Marumbi Matumbi

Band width of light spectrum [nm] Igombe Ruti Hippo Python Shadi Luanso male colourmale phenotype: – 1 (bottom) 5 (top)

arrows point to islands included in population genetic study on the left Magalhaes, Konijnendijk et al. unpubl. data Seehausen et al. 1997 Speciation reversal case 2: Lake Victoria cichlids

wavelength (nm) 400 500 600 700

100 a 30 1.0 a b 75 25 1 0.9 50 20 2 0.8 P. pundamilia P. nyererei 25 15 3 0 0.7 10 orange ratio

100 intensity light 6 b 0.6 75 5 9

50 (% of surface peak intensity) 0 0.5

light (% intensity of peak intensity) blue red 400 500 600 700 0246810 25 treatment treatment wavelength (nm) depth (m) 0 c Figure 2. Photic habitats in the study population at Makobe Island. IR light a) Transmission light spectra at different depths. Numbers indicate 16 16 * depth in meters. The dotted line indicates the 550 nm threshold 14 * which is used to calculate the orange ratio. b) The increase in 14 12 orange ratio with water depth. Shaded areas indicate P. pundamilia (0.5-2 m) and P. nyererei (4-7 m) breeding habitats. 12 projector r

sensitivity (steps) sensitivity 10 ro camera ir m pun nye pun nye Figure 3. Male nuptial coloration and female colour vison in Pundamilia. a) P. pundamila and P. nyererei males and females with the reflection spectra of male nuptial coloration. b) Transmission spectra of the blue and red light treatments used in the optomotor response test. c) The experimental setup and the performance of P. pundamilia (pun, n=14) and P. nyererei (nye, n=11) females. Left panel: blue light; right panel: red light. Boxes are medians with first and third quartiles, error bars indicate 10th and 90th percentiles. Asterisks: p<0.02. Maan et al. 2006 Speciation reversal case 2: Lake Victoria cichlids

Speciation reversal most likely accounts for some of the mass extinction of endemic cichlid fish in Lake Victoria Seehausen et al. 1997

n species in site

Seehausen et al. 1997 Speciation reversal case 2: Lake Victoria cichlids

Loss of species structure is associated with loss of ecological disparity and ecological diversity

ShoreDist (m) -75 -65 -55 -45 -35 -25 -15 -5 5 13.50 0

2 12.50

Depth (m) Depth 11.50 6 ShoreDist (m) blue Makobe, n=20 -75 -65 -55Fst -45= 0.029 -35 -25 -15 -58 5 red Makobe, n=56 0 10.50 P. "blue morph"

2 Luanso delta N15 P. "red morph" 9.50 4 Luanso P. nyererei 6 Makobe 8.50 blue Pyt hon, n=24 ShoreDist (m) P. pundamilia Fst = 0.008-0.021 8 -75red Pyt -65 hon, n=40 -55 -45 -35 -25 -15 -5 5 Makobe 0 P. pundamilia Python 7.50 2 P. pundamilia Python 4 P. pink anal 6.50 Depth (m) Depth 6 -19.00 -18.00 -17.00 -16.00 -15.00 -14.00 -13.00 -12.00 -11.00 blue Luanso, n=28 delta C13 Fst = 0.00 red Luanso, n=40 8 Mrosso et al. unpubl Speciation reversal case 3: Laurentian Great Lake Ciscoes

The pristine morphological disparity

Koelz 1929 Speciation reversal case 3: Laurentian Great Lake Ciscoes

Diversity decline in Lake Michigan due to size selective fishing and size selective predation by invasive sea lamprey …

1980s

… associated with morphological convergence: genetic admixture suspected Smith 1964 Speciation reversal case 3: Laurentian Great Lake Ciscoes

Now all but 2 species are reported extinct from the Great Lakes

artedi The last species pair, hoyi hoyi and artedi is allegedly strongly introgressed in Lakes Huron & Michigan

1917 1984/85

artedi hoyi relative frequency relative

number of gill rakers Todd & Stedman 1989 Steinhilber 2002 Speciation reversal case 3: Laurentian Great Lake Ciscoes

Loss of species structure here too is associated with loss of ecological disparity

Turgeon et al. characterized the ecological disparity in Lake Nippigon which still contains a subset of the Great Lake ciscoe diversity A = artedi B = zenithicus C = nigripinnis D = hoyi

Turgeon, Estoup, Bernatchez 1999 Speciation reversal case 4: Swiss Whitefish Radiation

Pascal Vonlanthen Speciation reversal case 4: Swiss Whitefish Radiation

Rapid loss of species diversity in the Swiss Whitefish radiation: 11 species and genetically distinct populations (~25%) went extinct in the past 50 years. Several others have converged morphologically, allegedly because of increased hybridization rates. This would seem one of the highest rates of vertebrate diversity loss but went largely unnoticed.

A sympatric benthic/pelagic pair with A sympatric overlapping benthic/pelagic spawning depth pair with distinct range spawning depth extant ranges extinct genetically extinct increasingly introgressed A changing adaptive landscape hypothesis

Hypoxic deepwaters select against deep water spawning

Size selective harvesting selects against large size Spawning depth

size Spawning depth hnigaatv adcp hypothesis adaptivelandscape A changing size hybridization as a source of diversity

Hybridization however, can generate new diversity when ecological opportunity is present Rieseberg et al. 2003 Science http://www3.botany.ubc.ca/rieseberglab/ Schwarz et al. 2005 Nature The Hawaiian silversword alliance, one of the most spectacular radiations of flowering plants, appears to be derived from a hybrid population between two or more species of North American tarweed. Barrier, M. et al. (1999) Interspecific hybrid ancestry of a plant adaptive radiation. Mol. Biol. Evol. 16, 1105-1113 A model of biodiversity dynamics with hybridization

Species-neutral model of biodiversity dynamics with hybridization

dR R(R −1) = sR(1− ω) − eR + h (1− 2ω) dt 2

Speciation Extinction Hybridization

R: number of species s: per capita speciation rate e: per capita extinction rate h: rate at which a pair of species produces a viable and fertile hybrid population ω: probability that a daughter/hybrid species genetically takes over a parental species A model of biodiversity dynamics with hybridization

dR R(R −1) = sR(1− ω) − eR + h (1− 2ω) dt 2

Parental Probability of re- Change Speciation species admixture in R

ω B’ 0 A AB 1-ω AB 1

R: number of species s: per capita speciation rate e: per capita extinction rate h: rate at which a pair of species produces a viable and fertile hybrid population ω: probability that a daughter/hybrid species takes over a parental species A model of biodiversity dynamics with hybridization

The ecological feedback loop: we assume overlap in mating system (hence ω) between species is ecology-dependent occurs more often with larger R and smaller H

Habitat heterogeneity (H) is low 1

R −1 ω = ω H + R −1

Habitat heterogeneity (H) is high 0 R A model of biodiversity dynamics with hybridization

dR R(R −1) = sR(1− ω) − eR + h (1− 2ω) dt 2

Parental Probability of re- Change Hybridization pair admixture in R ω2 C’ -1 ω(1- ω) AC’ 0 AB ACB (1-ω)ω C’B 0 (1-ω)2 ACB +1

R: number of species s: per capita speciation rate e: per capita extinction rate h: rate at which viable and fertile hybrid populations are produced ω: probability that a daughter/hybrid species takes over a parental species Equilibrium species richness, and the effect of hybridization depend on the relative rates of speciation and extinction: 3 different equilibrium regimes

I. s » e II. s ~ e III. s « e equilibrium dynamics equilibrium dynamics are are determined by s determined by h, which compensates for e-s»0, but fails to do so at small R

s = 4, e = 1, h = 1 s = 1.2, e = 1, h = 0.1 s = 1, e = 2, h = 2 s = per capita rate of speciation or, more generally, production of adaptive novelty e = per capita rate of extinction h = per capita rate of hybridization Effects of hybridization rate on equilibrium species richness in given environment s » e s ~ e s « e h can only reduce R equilibrium dynamics are h always increases R and subtle and very small larger h can compensate for changes in h can have e-s»0 at smaller R very large effects, it seems h always increases R

s = 4, e = 1 s = 1.2, e = 1 s = 1, e = 2 s = per capita rate of speciation or, more generally, production of adaptive novelty e = per capita rate of extinction h = per capita rate of hybridization Effects of environmental homogenization on equilibrium species richness s » e s ~ e s « e The size of the habitat The size of the habitat The size of the habitat homogenization effect on homogenization effect on homogenization effect on R R is smaller when R is much larger when h is not much affected by intrinsic h is already high is high (very small intrinsic h differences in h make a big difference)

1. The net effect of introgressive hybridization on species diversity depends on the environment

2. Unless speciation rates vastly exceed extinction rates, reduction in environmental heterogeneity precipitates collapse of diversity to a larger extent when introgression is common than when not. Because speciation rates by themselves decline as the heterogeneity of the environment declines, and intrinsic rates of hybridization (that were constant in our model) may increase, this is likely a serious threat to diversity.

3. In heterogenous environments, selection can in principle sort genetic diversity into ecological disparity. Gene exchange may by itself not be a threat to diversity, it may even generate diversity in such environments

4. Hybridization can alter biodiversity dynamics quantitatively and qualitatively and a thorough predictive framework is needed to understand its effects Policy Questions about Implications for Conservation

1. Do the findings of your research indicate a positive or negative secondary effect from evolutionary impacts on biological composition or the functionality of ecosystems ?

In most cases perhaps a negative secondary effect, namely biodiversity collapse though hybridization as a consequence of the homogenization of ecological landscapes and the associated evolutionary fitness landscapes. However, it really depends on the environmental context and properties of the biological system.

More rapid collapse of biodiversity where biodiversity is composed of complexes of species that can introgressively hybridize, e.g. high levels of neo-endemism. Policy Questions about Implications for Conservation

2. Do the findings of your research indicate that the human activities you are linking to evolutionary effect need to be further controlled or changed?

We have to increase awareness for the consequences of homogenization of the environment, and have to develop explicit measures of heterogeneity that allow to monitor its loss. Only then can measures be taken to control heterogeneity loss. We seem to lack strong conceptual foundations. Policy Questions about Implications for Conservation

3. Do you think that the findings of your research indicate that changing conservation practices could reduce the negative evolutionary effects of the human activities you studied?

Conservation may need to more actively incorporate measures to maintain the evolutionary processes by which species diversity arises. Specifically, we may want to think more about environmental determinants of ecological and genetic structure in biodiversity, and design conservation areas in ways to maintain these. Policy Questions about Implications for Conservation

4. Can you briefly describe any further research that you think might build on your findings to would in answering the questions above?

We need integrative theory development that builds on classical ecological (e.g. island biogeography) and evolutionary (e.g. speciation and adaptive radiation) theory and places these in an explicit environmental context. We also need much more molecular genetic data on gene exchange between species, particularly in animals.

Finally, we need to make some effort to characterize relevant heterogeneity (adaptive landscapes) that predict species diversity from ecological principles rather than just taking species diversity as a legacy of history. Hybridization and diversity dynamics

Many thanks to Co-authors: Gaku Takimoto, Jukka Jokela

PhD students: Collaborators: Alan Hudson Ruedi Müller Pascal Vonlanthen Denis Roy Martine Maan Jacques van Alphen Hilary Mrosso Vicky Schneider Isabel Magalhaes Salome Mwaiko Rike Stelkens

Funding: Swiss National Science Foundation (SNSF) EAWAG Thematic Focus “Aquatic Ecostystem” Dutch Science Foundation (WOTRO, ALW)