Thegenomics diversificationof organismal

Walter Salzburger Zoological Institute

Evolution

“The process by which different kinds of living organism are believed to have developed from earlier forms during the history of the earth.” The Oxford Advanced Learner’s Dictionary

!Charles R. Darwin (1809-1882) What is a species? distribution map

Bombina variegata

Bombina bombina

!Hybrid zone between yellow- and fire-bellied toad

What is a species?

Ensatina eschscholtzii ssp.

picta

platensis

oregonensis ring species croceater

xanthoptica

eschscholtzii klauberi Stebbins (1994) ! Ensantia eschscholtzii inhabits the western part of the USA What is a species?

‣ Individuals within a species are variable and there is usually no “ideal” or “typical” individual.

image: www.heliconius.org !Heliconius erato and H. melpomene are morphologically similar because of mimicry

Species concepts

‣ The category species is defined according to a species concept

biological A species is a group of interbreeding natural populations that is reproductively isolated species concept from other such groups (Mayr 1963).

cohesion A species is the most inclusive populations of individuals having the potential for species concept phenotypic cohesion through intrinsic cohesion mechanisms (Templeton 1989).

ecological A species is a lineages (or a closely related sets of lineages), which occupies an adaptive zone minimally different from that of any other lineage in range and which evolve species concept separately from all lineages outside its range (Van Valen 1976).

evolutionary A species is a single lineage of ancestral-descendant lineages that evolve separately from other such lineages and have their own evolutionary tendencies and historical fate species concept (Simpson 1961; Wiley 1978).

phylogenetic A species is the smallest monophyletic group of common ancestry (de Querioz & Donoghue 1988). A phylogenetic species is a basal cluster of organisms that is diagnosably distinct species concepts from other such clusters (Cracraft 1989)

Coyne & Orr (2004); Zachos 2016 Biological species concept

‣ Members of a species share a gene pool; selection and drift operate within species.

species X species Y

!Evolutionary biologists interpret species as independent evolutionary units

Biological species concept

‣ A species is a group of interbreeding natural populations that is reproductively isolated from other such groups (Mayr 1963).

♥

!The biological species concept places the category species within the framework of population genetics Reproductive isolation

species A

reproductive no partial complete isolation

ancestral species species B

speciation continuum

time

Reproductive isolation

locus under selection

species A divergence chromosome [position] disruptive divergence genome post-speciation selection hitchhiking hitchhiking divergence

ancestral species species B

speciation continuum

time

••• JL Feder, SP Egan & P Nosil (2012) TREE Reproductive isolation

isolating barrier

permeating postmating, prezygotic postzygotic

time

copulation fertilization

Geographic conditions allopatric speciation parapatric speciation sympatric speciation time Sympatric speciation

Amphilophus citrinellus Amphilophus zaliosus

lower pharyngeal jaw bone

Barluenga et al. (2006) Nature ! The Laguna de Apoyo is a small volcanic crater lake in Nicaragua

Parapatric speciation

Clinal models “Stepping-stone” models colonization

wet dry environmental gradient local adaptation

hybrid zone hybrid reproductive isolation Ecological speciation

‣ The evolution of reproductive isolation between populations by adaptation to different environments.

threespine stickleback

Jones et al. (2012) Nature ! Ecological speciation can happen in allopatry, parapatry and sympatry

Hybrid speciation

swamp freshwater marsh

Iris fulva hybrid Iris hexagona from: Arnold & Bennett (1993) ! Luisiana irises Polyploid speciation

diploid tetraploid (2n=4) (4n=8)

Natural selection

‣ ... is the process by which the forms of organisms in a population that are best adapted to the environment increase in frequency relative to less well-adapted forms over a number of generations (Ridley 2004)

images: www.idscaro.net, www.wikipedia.com Sexual selection

‣ … is the selection on mating behavior, either through: competition among members of one sex (usually males) for access to members of the other sex or through choice by members of one sex (usually females) for certain members of the other sex (Ridley 1996) www.smh.com.au , www.crbs.umd.edu images: images:

Natural selection Sexual selection

‣ Both natural and sexual selection operate if the following conditions are met:

reproduction organisms must reproduce to form new generations

heredity offspring resemble parents (“like must produce like”)

trait variation individuals in natural populations vary in (adaptive) traits

individuals in natural populations vary in the number of their variation in fitness offspring that survive to reproduce (‘lifetime reproductive success’) Natural selection Sexual selection

‣ There are fundamental difference between natural and sexual selection:

fitness competitors

sexual selection individual fitness other members of the same sex

natural selection fitness of the genotype other individuals in the same population

Natural variation

‣ Natural populations show variation at all levels, from gross morphology to DNA sequences. Selection can only operate, if heritable variation exists.

‣ Heritable natural variation is generated by two processes, mutation and recombination.

‣ New mutations are only transmitted to the next generation, if they occur in germinal tissue.

image: mun.ca Phenotypic evolution Molecular evolution genome phenome substitution nucleoide Met Asn ATG AACG “The primary causeofevolutionisthe “The primary Val T A TGGAGG... mutational changeofgenes” insertion/ TrpArg deletion heritable morphology morphology regulatory regulatory sequence structure behavior genome coding regions ecology ecology gene orgenome and/or and/or variation in: duplication Nei &

Kumar (2000) Met Asn ATG AACG Ala rearrangements C chromosome A TGGAGG... TrpArg Molecular evolution

Molecular evolution synonymous mutation: C > T

CCG CTT GTC AAC TAG GLY GLU GLN LEU ILE

non-synonymous mutation: A > C

CCG CTC GTC C AC TAG original DNA sequence: GLY GLU GLN ILE ILE CCG CTC GTC AAC TAG GLY GLU GLN LEU ILE frameshift mutation: insert C

CCG CCT CGT CAA CTA GLY GLY ALA VAL ASP

stop mutation: G > A

CCG CTC A TC AAC TAG GLY GLU STOP! Molecular evolution

‣ The rate of non-synonymous (dN) to synonymous (dS) substitution informs about the selective pressure that has acted on a protein coding gene:

dN/dS << 1: purifying selection

dN/dS = 1: neutrality

dN/dS > 1: positive selection (adaptive sequence evolution)

Molecular evolution

Ka/Ks = 4.026

‣ Pancreatic ribonuclease in colobine monkeys

douc langur

Zhang et al. (2002) Molecular evolution

‣ Pancreatic ribonuclease in leaf-eating monkeys

Prud’homme & Carroll (2006)

Zhang (2006)

Molecular evolution

‣ cis-regulatory evolution in fruitless

Gompel et al. (2005) Molecular evolution

‣ regulatory evolution in three spine sticklebacks

17% coding 41% regulatory

42% probably regulatory

Jones et al. (2012)

Chromosomal rearrangements

Recombination

chiasmata Chromosomal rearrangements

A B C D E F G H A B C D E F G H

deletion duplication

A E F G H A B C D E F G H F G H

A B C D E F G H A B C D E N O P Q R

reciprocal inversion translocation A E D C B F G H A B C O N E D P Q R

Chromosomal rearrangements

Chromosomal fission

A B C D E F G H I J

A B C D E F

G H I J Chromosomal rearrangements

Chromosomal fusion

A B C D E F G H I J

A B C D G H I J

Chromosomal rearrangements

‣ Chromosomal rearrangements in muntjac deers

Chinese muntjac deer

Indian muntjac deer

images: wdr.de, mun.ca Gene and genome duplications

‣ Hox gene clusters

Swalla (2006)

Gene and genome duplications

non-functionalization

original gene

original expression domain

“function” Gene and genome duplications

sub-functionalization

original gene

original expression domain

Gene and genome duplications

neo-functionalization

original gene

original expression domain

“function” Gene and genome duplications

‣ Caveats and pitfalls in phylogenetic inference: mixing paralogs with orthologs

species 1 species 2 species 3 1α 1β 2α 2β 3α 3β

orthologs (1α to 2α to 3α) (1β to 2β to 3β)

paralogs gene tree (e.g. 1α to 2β) species tree

gene duplication

Adaptive radiation images: Rich Glor images:

phenotype-environment correlation

common ancestry rapid speciation

trait utility Ecological opportunity

colonization extinction innovation

Cambrian explosion

‣ The ‘Cambrian evolutionary radiation’ most likely was an adaptive radiation.

trilobite www.field.ca image: image:

!The Burgess shale are fossil-rich deposits in the Yoho NP in British Columbia discovered by Charles D. Walcott in 1909 Cambrian explosion

Anomalocaris +

Pikaia (chordate)

Vauxia (sponge)

Wiwaxia +

Echmato- Ottoia crinus (priapulid) (echinoderm)

image: www.trilobites.info Helmetia Scenella (arthropod) (mollusk)

Extinction

‣ The ‘big five’ mass extinctions (based on marine fossils)

60 End-Permian Late Cambrian Late 40 End- Late Devonian Ordovician Triassic K-T Extinction 20

0 500 400 300 200 100 0

geological time (million years before present) Ca O S D C P Tr J K T

Sepkoski (1996), Rohde & Muller (2005) GenomesRadiating

Anolis

••• J Alföldi et al. (2011) Nature Heliconius

••• R Reed et al. (2011) Science

Heliconius

`

••• The Heliconius Genome Consortium (2012) Nature Stickleback

••• FC Jones et al. (2012) Nature

Darwin’s finches

••• S Lamichhaney et al. (2015) Nature Darwin’s finches

proportion of shared SNPs across the genome

100%

50% 100% astbur Astbur.:1-90001

50% Alignment 1 100% neobri Neobri. (-) 1-89776 Criteria: 70%, 100 bp 50% Regions: 61 20k 18k ••• Alignment 2 16k S Lamichhaney et al. (2015) Nature orenil 14k C7orf57 orenil. (+) 12k 13819-106755 10k Criteria: 70%, 100 bp 8k 100% Regions: 78 6k 4k 2k Alignment 3 0k psenye 50% psenye (+) 100% 9404-106232 Criteria: 70%, 100 bp Regions: 49 50% cichlidsX-axis: astbur 100% Resolution: 31 Window size: 100 bp gene exon 50% UTR 40k CNS 38k mRNA 36k 34k 32k 30k 28k 100% 26k 24k 22k Fhl2 (2of2) 20k 50% 100% C7orf57

50% 100%

50% 60k 58k 56k 54k 52k 50k 48k 46k 44k 42k 40k non-coding element divergence miRNAs

standing variation

gene duplication

transposable elements

••• D Brawand et al. (2014) Nature cichlids

SNP phylogenies

20.4 % 45.2 % 22.8 %

••• D Brawand et al. (2014) Nature radiating genomes

genomes gene duplications mobileelements regulatorychanges accelaratedcoding evolution miRNAs inversions hybridizationintrogressionILS

1 n/r YES maybe n/r n/r n/r n/a

5 YES YES YES YES YES n/r YES (>100)

1 n/r n/r n/r n/r n/r n/r YES (>100)

1 n/r YES maybe n/r YES n/r YES (>100)

1 n/r n/r YES n/r n/r YES YES (>100)

••• D Berner & W Salzburger (2015) Trends in Genetics