Macroevolution with a bite: Teeth evolution and diversification in ruminants

Macroevolution with a bite:

7HHWKHYROXWLRQDQGGLYHUVLÀFDWLRQLQ ruminants

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Dissertation presented for the degree of Philosophiae Doctor (PhD)

2018

Centre for Ecological and Evolutionary Synthesis Department of Biosciences

Faculty of Mathematics and Natural Sciences University of Oslo

©Olja Toljagić, 2018

Series of dissertations submitted to the

Faculty of Mathematics and Natural Sciences, University of Oslo No. 1998

ISSN 1501-7710

All rights reserved. No part of this publication may be

reproduced or transmitted, in any form or by any means, without permission.

Cover: Hanne Baadsgaard Utigard.

Print production: Reprosentralen, University of Oslo.

Preface

It gives me great pleasure to thank the many amazing people that made this thesis reality. I went into this odyssey without many preconceived notions of what it would entail, and I come out at the other side feeling grateful (and tired).

I have had incredible mentors, and I am indebted to all of them. Thomas F. Hansen – thank you for all the discussions, laughs, frustrations, advice, and knowledge you tried to instill in me. Any student is lucky to have you by their side and I feel very fortunate to have been working with you. I am especially thankful to you for teaching me to be uncompromising and think independently. Lee Hsiang Liow – your drive and quick thinking has kept me on my toes! Thank you for keeping my love for paleobiology alive and for the support throughout the years. Mikael Fortelius – your immense knowledge has been an incredible source of inspiration for me during our various trips together. Nils Christian Stenseth – you have created a unique work

environment, which has been one of the key things that made my life in Oslo so enjoyable. Thank you for always being extremely supportive of my endeavors.

Last, but certainly not least, Kjetil Lysne Voje – there are no words to express how grateful I am to you. You have been an absolutely fantastic mentor and friend. Thank you for the endless support, advice, patience, expertise, and thank you for the always uplifting words of wisdom!

I would like to thank my collaborators. Barbara Fischer, thank you for the support and enthusiasm at the beginning of my PhD life. Faysal Bibi – you once

–‘Ž†‡–Šƒ–‘’‡‹‰ƒ†”ƒ™‡”™‹–Šˆ‘••‹Ž–‡‡–Šˆ‘”–Š‡Ƥ”•––‹‡‹ƒ—•‡—

ˆ‡‡Ž•Ž‹‡›‘—Œ—•–ˆ‡ŽŽ‘˜‡”„‘ƒ”†‘ơ‘ˆƒ•Š‹’ƒ†›‘—…ƒǯ–•™‹ǤŠƒ›‘—ˆ‘”

throwing me a lifebelt! Michael Matschiner, thank you for teaching me how to build phylogenetic trees, and for your genuine interest and ideas surrounding my projects. Jostein Starrfelt, thank you for interesting discussions about macroevolution and life, and for the fantastic support. I would like to thank

–Š‡Ǯƒ…”‘‡˜‘Ž—–‹‘‰”‘—’ǯˆ‘”‡š…‡ŽŽ‡–†‹•…—••‹‘•ǡ•‘‡–‹‡•†—”‹‰–Š‡

journal club, sometimes over beer. Vesna Milankov has sparked my interest in evolution, and for that I am extremely thankful. The creators and coordinators

‘ˆ›Ǥ…Ǥ’”‘‰”ƒȋȌŠƒ˜‡„‡‡‹•–”—‡–ƒŽ‹›•Š‘”–•…‹‡–‹Ƥ… career so far, and I would especially like to thank Irma Knevel and Franjo Weissing for everything. I would not be where I am today, working with

’ƒŽ‡‘„‹‘Ž‘‰›ǡ‹ˆ‹–™ƒ•ǯ–ˆ‘”‹…Šƒ”†—–Ž‡”ǡ›Ƥ”•–Ǥ…Ǥ•—’‡”˜‹•‘”Ǥƒ

forever grateful to you for inviting me into the world of fossils, for being excited about macroevolution and for always being incredibly supportive! I would

also like to thank my other M.Sc. supervisors – Per Ahlbergh and Grzegorz

Niedzwiedzki for giving me a place in Uppsala where I could look at fossils. And

„”‡ƒ•‘‡‘ˆ–Š‡ǤŠ‡Ƥ”•–•–—†‡–•—’‡”˜‹•‡†ǡŒÞ”‘”‡‘’’‡”—†ǡ–Šƒ

you for all your hard work and teaching me how to be a supervisor.

I have met so many incredible people in Oslo, who have shaped my

experience here for the better! Thank you to Anders, Angelica, Anna, Cassie, ƒ„”‹…‡ǡ‡”ƒǡ‡‹†‹ǡ‡ŽŽ‡ǡ‡ƒƒǡ—‹•ǡƒ”ǡ‡”‹ŽŽ‡ǡ›ƒƒ†‘”‡Ǥ have enjoyed 17th of May, barbecues, weekends, and traveling with you guys,

›‘—ƒ”‡›”‘…•ǤŠƒ•ƒŽ•‘–‘›‹––‹‰…Ž—„ǡ›‘ƥ…‡ƒ–‡•‘˜‡”–Š‡

›‡ƒ”•ƒ†’‡‘’Ž‡ˆ‘”„‡‹‰ƒ‰”‡ƒ–…”‘™†–‘†”‹…‘ơ‡‡ǡ’ƒ”–›ǡƒ†

sometimes discuss science with. There are many people at CEES who have

Š‡Ž’‡†‡‘˜‡”–Š‡›‡ƒ”•ǡ‘‡™ƒ›‘”ƒ‘–Š‡”ǡƒ†…ƒǯ–’‘••‹„Ž›Ž‹•–›‘—ƒŽŽ„—–

I thank you from the bottom of my heart.

My friends who stuck with me over the years, while I was studying in

†‹ơ‡”‡–…‘—–”‹‡•Ȃ•‘‡‘ˆ›‘—Šƒ˜‡†‘‡‹–™‹–Š‡ǨŠƒ›‘—–‘ƒǡ

Bryn, Eileen, Ela, Emil, Filip, Filipe, Hector, Jelena, Katie, Kevin, Marija, Masha,

‹Žƒǡ‹Ž‹…ƒǡ‹…ƒ”†‘ƒ†”†ŒƒǤ‘’‡–‘‡‡–›‘—ƒ•‘ˆ–‡ƒ•’‘••‹„Ž‡

around the globe for new adventures.

My incredible family has been right there with me, through it all, mostly on Skype. I lost my grandma Ljubinka, but I know she would be so proud of me.

Sladjana, Zoran and Srdjan, you are the best team I could ever ask for, volim vas. Thank you for attempting to understand academia, to explain my work to people, and for patiently waiting for holidays so we can meet. This is for you.

Oslo, March 2018

‘‰”‡‡–‡ƒ…Š†ƒ›‘••‹Ƥ‡†Ǣ‹‡ˆ‘••‹Ž”‡ƒ‹•ˆ‘”‰‘––‡„‡‡ƒ–Š–Š‡

feet of something more lively.

Taylor Patton

Time is the longest distance between two places.

Tennessee Williams

© Ray Troll

Contents

List of papers...1

Summary...3

Introduction...5

—‹ƒ–•ǡ‰”ƒ••Žƒ†•ƒ†Š›’•‘†‘––‡‡–ŠǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤͣ Current debates surrounding hypsodonty evolution...11

Heavy lies the crown: Challenges in studying high-crowned fossil teeth...14

Hypsodonty: famous trait with infamous availability...14

Phylogenies and fossils...16

The papers...18

Concluding remarks and future perspectives...22

Acknowledgements...24

‡ˆ‡”‡…‡•ǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤǤ͞͡

Paper I Paper II Paper III

List of papers

Paper I

‘ŽŒƒ‰‹©ǡǤǡ‘Œ‡ǡǤǤǡƒ–•…Š‹‡”ǡǤǡ‹‘™ǡǤǡƬƒ•‡ǡǤ Ǥͣ͜͞͝Ǥ‹ŽŽ‹‘•

of years behind: Slow adaptation of ruminants to grasslands. Systematic biology 67: 145-157.

Paper II

‘ŽŒƒ‰‹©ǡ Ǥǡ ‘Œ‡ǡ Ǥ Ǥǡ –ƒ””ˆ‡Ž– Ǥ ͤ͜͞͝Ǥ Who is biting the dust? Dentition–

†‡’‡†‡– †‹˜‡”•‹Ƥ…ƒ–‹‘ †›ƒ‹…• ‹ ”—‹ƒ–•Ǥ Submitted to Journal of Evolutionary Biology.

Paper III

‘ŽŒƒ‰‹©ǡ Ǥǡ ‹‘™ǡ Ǥǡ ‘”–‡Ž‹—•ǡ Ǥ ͤ͜͞͝Ǥ ‘••‹Ž „‘˜‹† –‡‡–Š ”‡…‘”† ”‡ƪ‡…–•

polarized diet throughout the Late Neogene of Africa. Manuscript.

Summary

The tempo and mode of trait evolution is a long-lasting interest of

macroevolutionary research. Interactions between traits and the environment shape the astonishing biodiversity of life, and are therefore of interest for a number of questions of a broad evolutionary scope. This dissertation is about phenotypic evolution and adaptation on macroevolutionary time

•…ƒŽ‡•ǡƒ†–Š‡‡ơ‡…–‘ˆ‘”’Š‘Ž‘‰‹…ƒŽ–”ƒ‹–•‘†‹˜‡”•‹Ƥ…ƒ–‹‘†›ƒ‹…• in ruminating mammals. The particular focus is on the evolution of dental

–”ƒ‹–•ƒ††‹˜‡”•‹Ƥ…ƒ–‹‘†›ƒ‹…•ǡ‹”‡Žƒ–‹‘–‘–Š‡‰Ž‘„ƒŽƒ†˜ƒ…‡‡–‘ˆ

grasslands. Paper I reexamines the classic, as yet not fully resolved, story of adaptive evolution in deep time: the evolution of hypsodonty pertinent to the evolution of grasslands during the Cenozoic. We show that hypsodonty in ruminants evolved as an adaptation to both diet and habitat, at a slow, perhaps constrained, pace. Paper II investigates the interconnectedness of

Š›’•‘†‘–›‡˜‘Ž—–‹‘ƒ†”—‹ƒ–†‹˜‡”•‹Ƥ…ƒ–‹‘’ƒ––‡”•Ǥ‡Ƥ†–Šƒ–Š‹‰Š

speciation rates in ruminants are linked to increases in hypsodonty, owing to taxa with high-crowned teeth leaving more descendants, as opposed to transitions towards higher hypsodonty within lineages. Paper III examines a number of morphological traits on the crowns of bovid teeth in relation to dietary specialization and past environments. We show that bovid diets might have diverged towards two extremes, browsers and grazers, much earlier in the

‰”‘—’ǯ•Š‹•–‘”›–Šƒ’”‡˜‹‘—•Ž›–Š‘—‰Š–Ǥ

Introduction

Šƒ˜‡ƒ’’”‘ƒ…Š‡†ƒ˜‡”›„”‘ƒ†–‘’‹…Ȃ–”ƒ‹–‡˜‘Ž—–‹‘ƒ††‹˜‡”•‹Ƥ…ƒ–‹‘

– using phylogenetic comparative methods of trait adaptation, models of trait-

†‡’‡†‡–†‹˜‡”•‹Ƥ…ƒ–‹‘ǡƒ†…Ž—•–‡”‹‰ƒ’’”‘ƒ…Š‡•ƒ’’Ž‹‡†–‘ˆ‘••‹Ž†ƒ–ƒǤ Although I often feel like a “Jack of all trades, is a master of none”, it is my belief that questions involving macroevolutionary patterns are best addressed broadly. To quote G. G. Simpson (1944), my hope is that: “The intention will hardly be criticized, whatever is said about its execution.”

ƒ…”‘‡˜‘Ž—–‹‘ǡ˜‡”›„”‘ƒ†Ž›†‡Ƥ‡†ǡ‹•–Š‡•–—†›‘ˆ‡˜‘Ž—–‹‘‘……—””‹‰

at species level or above, across large time scales (Stanley 1979). Historically,

ƒ…”‘‡˜‘Ž—–‹‘Šƒ•„‡‡•–—†‹‡†—•‹‰–™‘˜‡”›†‹ơ‡”‡–ƒ’’”‘ƒ…Š‡•

ȋŽƒ–‡”Ƭƒ”‘͜͟͞͝ȌǤ‡‹•–Š‡—•‡‘ˆ’ƒŽ‡‘–‘Ž‘‰‹…ƒŽ†ƒ–ƒ‹ƒ††”‡••‹‰

questions relating to evolutionary dynamics and trends over substantial periods of time, while the other uses extant taxa and comparative methods to address the same questions, and can be applied to considerably shorter time scales. One major challenge in studies of evolutionary patterns and processes occurring on macroevolutionary time scales has been the merging

‘ˆ–Š‡–™‘ƒˆ‘”‡‡–‹‘‡†ƒ’’”‘ƒ…Š‡•ǤŠ‡Ƥ‡Ž†Šƒ•„‡‡Ƥ–‡†–”‡‡†‘—•Ž›

ˆ”‘ƒ‹–‡”•‡…–‹‘ƒŽƒ’’”‘ƒ…Šȋƒ„Ž‘•‹ͥ͜͜͞Ȍ‡˜‡”•‹…‡–Š‡Ƥ”•–‡ơ‘”–•

to synthesize paleontology and genetics (Simpson 1944). Great progress has been made in bringing molecular biology and paleontology together also due to the expansion of modern statistical modelling and the ongoing genomic

”‡˜‘Ž—–‹‘ȋƒ„Ž‘•‹ƬŠ—„‹͜͞͝͡ȌǤŠ‹Ž‡ƒ›…ŠƒŽŽ‡‰‡•”‡ƒ‹ǡ’”‡•‡–Ž›

one of the main interests of macroevolutionary research lies at the intersection of phylogenetics and paleontology, e.g.: time-scaling phylogenies, studying

’Š‡‘–›’‹…‡˜‘Ž—–‹‘ǡƒ†‘†‡ŽŽ‹‰•’‡…‹‡•†‹˜‡”•‹Ƥ…ƒ–‹‘†›ƒ‹…•ȋ‡‡ŽŽ

Ƭƒ”‘͜͟͞͝Ǣƒ„Ž‘•‹ƬŠ—„‹͜͞͝͡Ǣ—–ƬŽƒ–‡”͜͢͞͝ȌǤŠ‡“—‡•–‹‘•

of how much and how fast phenotypes change over time, and how this in turn

ƒơ‡…–•†‹˜‡”•‹Ƥ…ƒ–‹‘ȋ•’‡…‹ƒ–‹‘ǡ‡š–‹…–‹‘Ȍ”ƒ–‡•ǡƒ”‡ƒ…”—…‹ƒŽ’ƒ”–‘ˆ–Š‡

research on broad-scale evolutionary patterns. This dissertation examines some

ƒ•’‡…–•‘ˆ–Š‡•‡“—‡•–‹‘•Ǣƒ‹Ž›–Š‡’ƒ––‡”ƒ†–‡’‘‘ˆ–”ƒ‹–‡˜‘Ž—–‹‘ǡƒ†

†‹˜‡”•‹Ƥ…ƒ–‹‘†›ƒ‹…•ǡƒŽŽ‘‹ŽŽ‹‘Ǧ›‡ƒ”–‹‡•…ƒŽ‡•Ǥ

The comparative method has been one of the leading tools in the investigation of trait adaptation. With the increase in the availability and volume of molecular data, and the proliferation of more sophisticated tree- building methods, we have gained access to a large number of increasingly

”‘„—•–’Š›Ž‘‰‡‡–‹…–”‡‡•ˆ‘”ƒ›…Žƒ†‡•ȋ‡‡ŽŽƬƒ”‘͜͟͞͝Ǣ—–Ƭ Slater 2016). Simultaneously, advances in modern phylogenetic comparative methods, which are used to test hypotheses of adaptation, have allowed us to

†‡Ž˜‡‹–‘–Š‡Žƒ”‰‡Ǧ•…ƒŽ‡’ƒ––‡”•‘ˆ„‹‘†‹˜‡”•‹–›ȋƒ•‡͜͞͝͠Ǣ—–ƬŽƒ–‡”

2016). As a part of this dissertation, I employ such phylogenetic comparative methods to investigate the speed of adaptation of high-crowned (hypsodont)

–‡‡–Š‹”—‹ƒ–•’‡…‹‡•‹”‡Žƒ–‹‘–‘‡š’‘•—”‡–‘†‹ơ‡”‡–‹…Š‡•

(environments) with diverse selective pressures. I also include information from the fossil record of grasslands to inform the timeline of hypsodonty evolution.

‡š–—•‡–”ƒ‹–Ǧ„ƒ•‡†…‘’ƒ”ƒ–‹˜‡‡–Š‘†•ˆ‘”†‹˜‡”•‹Ƥ…ƒ–‹‘–‘ƒƒŽ›œ‡–Š‡

‹ƪ—‡…‡‘ˆŠ›’•‘†‘–›‘”—‹ƒ–†‹˜‡”•‹Ƥ…ƒ–‹‘Ǥ‡…‡–†‡˜‡Ž‘’‡–•‘ˆ

methods for state-dependent speciation and extinction (reviewed in Morlon

2014) allowed for simultaneous accounting of trait evolution with speciation

ƒ†‡š–‹…–‹‘”ƒ–‡•ǤŠ‹•‰”‘—’‘ˆ‡–Š‘†•ȋƒŽ•‘…ƒŽŽ‡†–Š‡Ǯ‡–Š‘†•ǯȌ supports the investigation of the complex interaction between traits and

†‹˜‡”•‹Ƥ…ƒ–‹‘”ƒ–‡•ǡ™Š‹…Š‹•‡›ˆ‘”†‹•‡–ƒ‰Ž‹‰–Š‡‡ơ‡…–•–Šƒ––Š‡•‡

interactions have on the evolution of clades on macroevolutionary time-scales ȋ‡‡ŽŽƬƒ”‘͜͟͞͝ȌǤ

Another way to examine large-scale patterns is to directly examine fossils and their morphologies through time. Paper III characterizes morphological change of the dentitions of bovid fossil taxa through the past 7 million years in Africa, in relation to dietary preferences and environmental conditions. Using clustering methods, we tested how morphological traits, environmental traits, or both, associate with the distribution of taxa through time. The emerging patterns of the clustering of taxa through time allow us to hypothesize about

†‹ơ‡”‡–•‡Ž‡…–‹˜‡’”‡••—”‡•–Šƒ–…‘—Ž†Šƒ˜‡‹ƪ—‡…‡†–Š‡‡˜‘Ž—–‹‘‘ˆ–Š‡

examined trait. Additionally, by using the resulting clusters in regression models, we could evaluate how well past environments predict these clusters of taxa. This could be of interest in the study of ecometrics, which employs morphological traits of fossil taxa as proxies for past environments (e.g. Eronen et al. 2010).

Ruminants, grasslands and hypsodont teeth

—‹ƒ–•ƒ”‡ƒ•—„‘”†‡”‘ˆ‡–ƒ”–‹‘†ƒ…–›Žƒ–Šƒ–‹…Ž—†‡•ƒ”‘—†͜͜͞

‡š–ƒ–ƒ†”‡…‡–Ž›‡š–‹…–•’‡…‹‡•‹•‹šˆƒ‹Ž‹‡•ȋ”ƒ‰—Ž‹†ƒ‡ǡ‹”ƒƥ†ƒ‡ǡ

–‹Ž‘…ƒ’”‹†ƒ‡ǡ‘•…Š‹†ƒ‡ǡ‡”˜‹†ƒ‡ǡƒ†‘˜‹†ƒ‡Ȍȋ ‡”ž†‡œƬ”„ƒ͜͜͞͡ȌǤ

Š‡›ƒ”‡‘‡‘ˆ–Š‡‘•–†‹˜‡”•‡‰”‘—’•‘ˆŽƒ”‰‡–‡””‡•–”‹ƒŽƒƒŽ•Ǣ–Š‡›•’ƒ

most continents (except Australia and Antarctica) and are morphologically, ecologically, physiologically, and behaviorally diverse. Their rich fossil record and high present-day diversity represent a great asset for understanding evolutionary processes. My research focuses on ruminant dental evolution in relation to the spread of grasslands, as ruminants are the dominant herbivores of contemporary terrestrial open habitats, cover a range of diets, and have

†‡˜‡Ž‘’‡†˜ƒ”›‹‰†‡‰”‡‡•‘ˆŠ›’•‘†‘–›ȋ”„ƒƬ…ŠƒŽŽ‡”͜͜͜͞ȌǤ

Grasses (Poacea) make up one of the most dominant contemporary biomes – grasslands, which have been expanding since the Late Cretaceous, replacing forests on most continents (Figure 1). The spread of grasslands in mid-Cenozoic and the subsequent independent attainment of hypsodonty in ungulate

Ž‹‡ƒ‰‡•ȋŠ‘‘ˆ‡†ƒƒŽ•Ȍƒ†‘–Š‡”Š‡”„‹˜‘”‡•ȋ•„‘”ͥ͜͝͝Ǣ‹’•‘ͥ͝͠͠Ǣ

ƒƒŽ‡ͥ͢͜͝Ǣƒ‹•ͥͤͤ͝Ǣƒ‹•Ƭ ‘”–‡Ž‹—•ͥͤͤ͝Ǣƒ… ƒ††‡ͥͥ͝͞Ǣ”‡˜‹‡™‡†

‹ƒ—–ŠƬƒ‹•͜͞͝͝Ȍ‹•ƒ…Žƒ••‹…•–‘”›‘ˆƒ†ƒ’–‹‘ǤŽ‘„ƒŽ…‘‘Ž‹‰ƒ†ƒ•Š‹ˆ–

from low to high seasonality purportedly led to grassland expansion (Jacobs

‡–ƒŽǤͥͥͥ͝Ǣ†™ƒ”†•‡–ƒŽǤ͜͜͞͝Ǣ–”ڏ„‡”‰͜͞͝͝ȌǤŠ‡”‡™‡”‡•‡˜‡”ƒŽ‹’‘”–ƒ–

•–ƒ‰‡•‹–Š‡‡˜‘Ž—–‹‘ƒ”›Š‹•–‘”›‘ˆ‰”ƒ••Žƒ†•ƒ……‘”†‹‰–‘–”ڏ„‡”‰ȋ͜͞͝͝Ȍǣ DzȋƒȌ–Š‡ƒŽ‡‘‰‡‡ƒ’’‡ƒ”ƒ…‡‘ˆ͟‘’‡ǦŠƒ„‹–ƒ–‰”ƒ••‡•Ǣȋ„Ȍ–Š‡ƒŽ‡‘‰‡‡

ƒ’’‡ƒ”ƒ…‡‘ˆ͠‘’‡ǦŠƒ„‹–ƒ–‰”ƒ••‡•Ǣȋ…Ȍ–Š‡‹†ǦŽƒ–‡‡‘œ‘‹…‡‡”‰‡…‡

‘ˆ‘’‡ǡ͟‰”ƒ••Ǧ†‘‹ƒ–‡†Šƒ„‹–ƒ–•Ǣƒ†ƤƒŽŽ›ǡ‹•‘‡”‡‰‹‘•ǡȋ†Ȍ–Š‡Žƒ–‡

Neogene shift to C4-dominated grass-dominated habitats.” Importantly, the

–‡’‘”ƒŽ’ƒ––‡”•‘ˆ–Š‡•‡•–ƒ‰‡•†‹ơ‡”†‡’‡†‹‰‘–Š‡…‘–‹‡–‘””‡‰‹‘Ǥ

As a result, the origin and subsequent rise to dominance of grasslands has

„‘–Šƒơ‡…–‡†–Š‡‡˜‘Ž—–‹‘‘ˆŠ‡”„‹˜‘”‡•ƒ†Šƒ†ƒ•–”‘‰‹ƪ—‡…‡‘‰Ž‘„ƒŽ

…Ž‹ƒ–‡–Š”‘—‰Š–Š‡…ƒ”„‘ƒ†•‹Ž‹…ƒ…›…Ž‡•ȋ–”ڏ„‡”‰͜͞͝͝ȌǤ

Figure 1: ”ƒ••Žƒ†‹–Š‡ƒƒ•ƒ‹ƒ”ƒƒ–‹‘ƒŽ‡•‡”˜‡ǡ‡›ƒǡˆ”‹…ƒǤ

Evolution of herbivory is connected to a number of adaptations in

morphology, physiology and behavior of herbivorous mammals (e.g. Demment Ƭƒ‘‡•–ͥͤ͝͡ȌǤ’ƒ”–‹…—Žƒ”ǡ…”ƒ‹‘Ǧ†‡–ƒŽƒ†ƒ’–ƒ–‹‘•‹—‰—Žƒ–‡•Šƒ˜‡

”‡…‡‹˜‡†—…Šƒ––‡–‹‘ȋ‡Ǥ‰Ǥƒ‹•ͥͥ͝͡Ǣƒ‹•Ƭ ‘”–‡Ž‹—•ͥͤͤ͝Ǣ‡†‘œƒ‡–ƒŽǤ 2002), especially the aforementioned evolution of hypsodonty. The assumption is that hypsodonty was an adaptation to feeding on a new abrasive food source (grasses containing silica) in a new niche – open and arid habitats (Fortelius

ͥͤ͝͡Ǣƒ‹•ͥͤͤ͝Ǣƒ‹•Ƭ ‘”–‡Ž‹—•ͥͤͤ͝Ǣƒ—–ŠƬƒ‹•͜͞͝͝Ǣƒ”†‹‡‡–ƒŽǤ͜͞͝͞ȌǤ The crown of hypsodont teeth (usually molars, less often premolars) has been vertically elongated in comparison to the ancestral condition, brachydonty ȋ ‹‰—”‡͞Ȍȋƒ—–ŠƬƒ‹•͜͞͝͝ȌǤƒŠ›’•‘†‘––‘‘–Š•‘‡’‘”–‹‘‘ˆ–Š‡

crown is retained within the jaw to erupt later in life, unlike in the brachydont teeth where the whole crown is above the level of the jawbone on initial

‡”—’–‹‘ȋƒ—–ŠƬƒ‹•͜͞͝͝ȌǤŠ‹•‡Ž‘‰ƒ–‹‘‹•Š›’‘–Š‡•‹œ‡†–‘’”‘Ž‘‰–Š‡

life-span of an animal, because there is more tooth material to wear (e.g. Kurtén

ͥ͟͝͡ǢƒƒŽ‡ͥ͢͜͝ǡͥ͢͝͠Ǣ ‘”–‡Ž‹—•ͥͤ͝͡Ǣƒ‹•ͥͤͤ͝ȌǤ‡…ƒ—•‡‘ˆ–Š‹•ƒ†ƒ’–‹˜‡

Š›’‘–Š‡•‹•ƒ†–Š‡ˆƒ…––Šƒ––‘‘–Š‘”’Š‘Ž‘‰›”‡ƪ‡…–•–Š‡ˆ‡‡†‹‰Šƒ„‹–•‘ˆ

ƒ‹ƒŽ•ȋ—–Ž‡”ͥͤ͟͝Ǣ ‘”–‡Ž‹—•ͥͤ͝͡Ǣ–”ڏ„‡”‰͜͜͢͞ȌǡŠ›’•‘†‘–›Šƒ•„‡‡

—•‡†ƒ•ƒ–‘‘Žˆ‘”‹ˆ‡””‹‰’ƒ•–†‹‡–•ƒ†‡˜‹”‘‡–•ȋ”‘‡‡–ƒŽǤ͜͜͞͝„Ǣ

•‡‡ƒ—–ŠƬƒ‹•͜͞͝͝ˆ‘”ƒ‘˜‡”˜‹‡™ȌǤ‘™‡˜‡”ǡ‹–Šƒ•„‡‡•—‰‰‡•–‡†–Šƒ–

hypsodonty needs to be supplemented with other cranial and tooth measures

–‘ƒ†‡“—ƒ–‡Ž›’”‡†‹…–†‹‡–•ȋƒ‹•ͥͤͤ͝Ǣ ‘”–‡Ž‹—•Ƭ‘Ž‘—‹ƒ•͜͜͜͞ȌǤ

A number of other techniques have been developed to study tooth-wear

ƒ††‹‡–Ǣ‹…”‘™‡ƒ”ȋ‡Ǥ‰Ǥ‘Ž‘—‹ƒ•‡–ƒŽǤͥͤͤ͝Ȍǡ‡•‘™‡ƒ”ȋ ‘”–‡Ž‹—•Ƭ

Solounias 2000), and measuring the isotopic content of enamel (MacFadden Ƭ‡”Ž‹‰ͥͥ͝͠Ȍǡ–‘‡–‹‘‘Ž›ƒˆ‡™Ǥ‘–Š‹…”‘™‡ƒ”ƒ†‡•‘™‡ƒ”ƒ”‡

measures of tooth-wear during a lifetime of an animal, and hence operate

‘†‹ơ‡”‡––‹‡•…ƒŽ‡•–ŠƒŠ›’•‘†‘–›Ǥ‡ƒ•—”‹‰…ƒ”„‘‹•‘–‘’‡•‹

tooth enamel is used in distinguishing between diets of plants with C4

˜‡”•—•͟’Š‘–‘•›–Š‡•‹•ȋ’”‡•—ƒ„Ž›”‡ƪ‡…–‹‰‰”ƒ••˜‡”•—•„”‘™•‡†‹‡–ǡ respectively). Hence, this technique is most useful in the context of Late Miocene transition to C4 grasses, and is additionally more invasive compared

to the aforementioned measurements since it usually requires drilling a specimen.

Figure 2: Longitudinal sections of cheek teeth. (A) Low-crowned, or brachydont tooth (human molar). (B) High-crowned, or hypsodont tooth (horse molar).

‹‰—”‡‘”‹‰‹ƒŽŽ›’—„Ž‹•Š‡†„›–”ڏ„‡”‰͜͜͢͞ȋ‘†‹ˆ‹‡†ˆ”‘ƒ‹•Ƭ ‘”–‡Ž‹—•

ͥͤͤ͝ǡ‘”‹‰‹ƒŽŽ›ˆ”‘–‡‡ŽƬƒ”˜‡›ͥͣͣ͝ȌǤ

Current debates surrounding hypsodonty evolution

The evolution of hypsodont teeth is a continuous source of debate galvanized

„›‡™‡–Š‘†‘Ž‘‰‹‡•ƒ†”‡Ǧ‡˜ƒŽ—ƒ–‹‘‘ˆ‘Ž†Š›’‘–Š‡•‡•ȋ‡Ǥ‰Ǥ‡†‘œƒƬ

ƒŽ“˜‹•–ͤ͜͜͞Ǣƒ—–ŠƬƒ‹•͜͞͝͝Ǣƒ”†‹‡‡–ƒŽǤ͜͞͝͞ȌǤ‡Ž‘‰Ǧ•–ƒ†‹‰

†‡„ƒ–‡…‘…‡”•–Š‡‹ƪ—‡…‡‘ˆ†‹ơ‡”‡–…ƒ—•ƒ–‹˜‡ƒ‰‡–•‘ˆ–‘‘–Š™‡ƒ”ǡƒ†

has been focused mainly around the polarizing views of “grass versus grit”.

Some researchers have argued that the main cause of tooth wear in herbivores

‹•†—‡–‘–Š‡‹ƪ—‡…‡‘ˆ–Š‡‹Š‡”‡–’”‘’‡”–‹‡•‘ˆ‰”ƒ••‡•ȋ•—…Šƒ•Šƒ”†•‹Ž‹…ƒ

„‘†‹‡•…ƒŽŽ‡†’Š›–‘Ž‹–Š•Ȍǡ™Š‹Ž‡‘–Š‡”•ˆ‘…—•‡†‘–Š‡‡ơ‡…–•‘ˆ–Š‡‹‰‡•–‹‘

of soil particles when feeding close to the ground in open habitats (reviewed

‹ƒ—–ŠƬƒ‹•͜͞͝͝ȌǤ‡•’‹–‡–Š‡‘‰‘‹‰†‡„ƒ–‡•ƒ†–Š‡’‘•–—Žƒ–‹‘

of hypsodonty as an adaptation causing evolutionary trends over long-time scales, only a handful of studies have examined this in an explicit phylogenetic …‘’ƒ”ƒ–‹˜‡ˆ”ƒ‡™‘”ȋƒ•‡ͥͥͣ͝Ǣ‹ŽŽ‹ƒ•Ƭƒ›͜͜͞͝Ǣ–”ڏ„‡”‰͜͜͢͞ȌǤ This prompted me to address the adaptive evolution of hypsodonty in the light

‘ˆ†‹ơ‡”‡–†‡–‡”‹ƒ–•ǡ—•‹‰”‹‰‘”‘—•‘†‡”’Š›Ž‘‰‡‡–‹……‘’ƒ”ƒ–‹˜‡

methods. These methods allowed me to address the timeline of hypsodonty evolution in relation to grassland expansion, as well as the apparent “adaptive lag” between the appearance of grasslands and the evolution of highly

Š›’•‘†‘–ˆ‘”•‹–Š‡ˆ‘••‹Ž”‡…‘”†ȋƒ•‡ͥͥͣ͝Ǣ‹ŠŽ„ƒ…ŠŽ‡”Ƭ‘Ž‘—‹ƒ•

͜͜͢͞Ǣ–”ڏ„‡”‰͜͜͢͞Ǣƒ—–ŠƬƒ‹•͜͞͝͝Ǣ‹ŠŽ„ƒ…ŠŽ‡”‡–ƒŽǤ͜͞͝͝ȌǤ

Another controversy is the persistence of brachydont forms, which remain …‘‘‹’”‡•‡–Ǧ†ƒ›—‰—Žƒ–‡ˆƒ—ƒ•ȋƒ—–ŠƬƒ‹•͜͞͝͝ȌǤ”‡ƒ•‘

•‘‡Ƥ†–Š‹•–‘„‡—‡š’‡…–‡†ȋ‡Ǥ‰Ǥ ‡”ƒ‡…ͣ͜͜͞Ǣ‹˜ƒŽ•‡–ƒŽǤ͜͜͞͝Ȍ‹•–Š‡

perhaps the underlying assumption that hypsodonty is superior to brachydonty ȋƒ—–ŠƬƒ‹•͜͞͝͝ȌǤ˜‡–Š‘—‰Šƒ›—‰—Žƒ–‡•‡˜‘Ž˜‡†‹…”‡ƒ•‡†

hypsodonty, this did not seem to be a case of hypsodont taxa completely

replacing brachydonts (Janis et al. 2000). This led me to examine the pattern of

”—‹ƒ–†‹˜‡”•‹Ƥ…ƒ–‹‘‹–Š‡Ž‹‰Š–‘ˆ–”ƒ•‹–‹‘•ˆ”‘„”ƒ…Š›†‘––‘Š‹‰ŠŽ›

Š›’•‘†‘–ˆ‘”•Ǥ—‹ƒ–Š›’•‘†‘–›‡˜‘Ž—–‹‘ƒ††‹˜‡”•‹Ƥ…ƒ–‹‘Šƒ˜‡ǡ until now, been examined separately. In Paper II we investigate these jointly,

using a set of comparative state-dependent speciation and extinction (SSE)

‡–Š‘†•ȋƒ††‹•‘‡–ƒŽǤͣ͜͜͞Ǣ ‹–œ‘Š͜͜͞͝ǡ͜͞͝͞Ǣ‡ƒ—Ž‹‡—Ƭǯ‡ƒ”ƒ͜͢͞͝ȌǤ These methods circumvent the problem of mistaking a bias in evolutionary

”ƒ–‡•ȋ–”ƒ•‹–‹‘•Ȍ‘ˆƒ–”ƒ‹–ˆ‘”ƒ†‹ơ‡”‡…‡‹†‹˜‡”•‹Ƥ…ƒ–‹‘”ƒ–‡•ȋǯ‡ƒ”ƒ

Ƭ‡ƒ—Ž‹‡—͜͢͞͝ȌǤ‡ƒ’’Ž‹‡††‹ơ‡”‡––›’‡•‘ˆ–Š‡ˆƒ‹Ž›‘ˆ‡–Š‘†•–‘

‹˜‡•–‹‰ƒ–‡Š›’•‘†‘–›ƒ•„‘–Šƒ…ƒ–‡‰‘”‹…ƒŽƒ†…‘–‹—‘—•–”ƒ‹–ƒơ‡…–‹‰

–Š‡’ƒ––‡”‘ˆ†‹˜‡”•‹Ƥ…ƒ–‹‘‹”—‹ƒ–•ǡ™Š‹Ž‡ƒŽ•‘–‡•–‹‰ˆ‘”’‘–‡–‹ƒŽ

ƒ††‹–‹‘ƒŽŠ‹††‡˜ƒ”‹ƒ„Ž‡•ƒơ‡…–‹‰–Š‡–”ƒ‹–Ǥ

Lastly, hypsodonty has been used as an environmental signal of habitat

•–”—…–—”‡ǡ”‡ƪ‡…–‹‰˜‡‰‡–ƒ–‹‘ƒ†‘’‡‡••‘ˆŠƒ„‹–ƒ–ȋƒ—–Š‡–ƒŽǤ

͜͜͞͞Ǣƒ‹•‡–ƒŽǤ͜͜͞͠Ǣ”‘‡‡–ƒŽǤ͜͜͞͝„ȌǤ‹…‡Š›’•‘†‘–›Šƒ•„‡‡–‹‡†

to an adaptive lag, the existence of this time-lag in trait adaptation should

„‡–ƒ‡‹–‘ƒ……‘—–™Š‡Š›’•‘†‘–›‹•—•‡†ƒ•ƒ’”‘š›ˆ‘”†‹ơ‡”‡–

’ƒŽ‡‘‡˜‹”‘‡–•ƒ†…Ž‹ƒ–‡•ȋ–”ڏ„‡”‰͜͜͢͞Ǣ‘ŽŒƒ‰‹©‡–ƒŽǤͣ͜͞͝ȌǤ

††‹–‹‘ƒŽŽ›ǡ‡ƒ•—”‡•‘ˆŠ›’•‘†‘–›ƒ”‡†‹ƥ…—Ž––‘ƒ…“—‹”‡‹–Š‡ˆ‘••‹Ž”‡…‘”†

(see section on challenges in studying high-crowned fossil teeth). This led me to explore a number of morphological traits on the tooth-crown of ruminant fossil teeth based on dietary adaptations. I used clustering methods to examine the grouping of morphological traits in a fossil series of African bovids

spanning around 7 million years and tested hypotheses of the environmental impact on these groupings. The resulting morphological clusters were then used to assess how well the environmental variables predict these clusters. This can give an idea of the possibility of using these as environmental signals in the study of ecometrics (Eronen et al. 2010).

Heavy lies the crown: challenges in studying high-crowned fossil teeth

Hypsodonty: famous trait with infamous availability

Hypsodonty has evolved many times independently among mammals, both in the extinct multituberculates and within marsupials and placentals (Damuth Ƭƒ‹•͜͞͝͝ȌǤ”–‹‘†ƒ…–›Žƒƒ†‡”‹••‘†ƒ…–›ŽƒƒŽ‘‡ǡŽ‹˜‹‰ƒ†‡š–‹…–ǡ

hypsodonty evolved at least 17 times in addition to its repeated evolution in

ˆƒ‹Ž‹‡••—…Šƒ•–Š‡‘˜‹†ƒ‡ȋƒ‹•Ƭ ‘”–‡Ž‹—•ͥͤͤ͝Ǣƒ—–ŠƬƒ‹•͜͞͝͝ȌǤ The present consensus is that evolution of hypsodonty was associated with either abrasive diet (e.g. grasses, plant roots) and/or ingesting large amounts of soil (e.g. feeding at ground level in open habitats, subterranean foraging).

……‘”†‹‰–‘ƒ—–ŠƬƒ‹•ȋ͜͞͝͝ȌǣDz›’•‘†‘–›•Š‘—Ž†„‡†‡Ƥ‡†ǡ‘–„›

any relative dental measurement, but by the condition where the base of the crown of the newly erupted tooth lies within the bone of the jaw, rather than the junction between crown and root occurring at the level of the jaw bone (= the gum line in life), as is the condition in most mammals.” This trait has

–”ƒ†‹–‹‘ƒŽŽ›„‡‡“—ƒ–‹Ƥ‡†™‹–ŠƒŠ›’•‘†‘–›‹†‡šǡƒ†ˆ‘”…‘˜‡‹‡…‡

”‡•‡ƒ”…Š‡”•‘ˆ–‡†‡Ƥ‡††‹ơ‡”‡–†‡‰”‡‡•‘ˆŠ›’•‘†‘–›Ǥ›™‘”Šƒ˜‡

ˆ‘…—•‡†‘–Š‡Š›’•‘†‘–›‹†‡š†‡Ƥ‡†„›ƒ‹•ȋͥͤͤ͝Ȍƒ•Dz–Š‡—™‘”

M3 crown height divided by the occlusal width of the same tooth”, and the

†‡Ƥ‹–‹‘••Š‡’”‘’‘•‡†‘ˆ–Š‡Dz†‡‰”‡‡•‘ˆŠ›’•‘†‘–›dz„ƒ•‡†‘–Š‹•‹†‡š

(see Papers I and II).

Š‡Ƥ”•–…‘’”‡Š‡•‹˜‡•‡–‘ˆ‡ƒ•—”‡•‘ˆŠ›’•‘†‘–›‹†‹…‡•ˆ‘”‡š–ƒ–

ungulates comes from Janis (1988). It includes X-rays of the jaws of hypsodont

ƒ‹ƒŽ•ƒ†”‡ƒ‹•–Š‡‘•–‡šŠƒ—•–‹˜‡†ƒ–ƒ•‡––‘†ƒ–‡ǤŠ‡†‹ƥ…—Ž–›‹

measuring hypsodonty index comes from the fact that it needs to be measured

‘—™‘”‘Žƒ”–‡‡–Šǡƒ†–Š‘•‡ƒ”‡†‹ƥ…—Ž––‘…‘‡ƒ…”‘••‹–Š‡ˆ‘••‹Ž

record – an adult animal needed to be fossilized before wearing its molars!

As an illustration of this problem, I have collected data on more than 300

specimens of fossil bovids from the Nairobi Natural History Museum collection (some of these data are used in Paper III). Although this is a comprehensive fossil collection spanning around 8 million years back in time, I encountered fewer than 5 specimens of unworn molars on which I could measure

hypsodonty index (Figure 3). This is one of the reasons why we analyze a

number of other crown traits on in Paper III. Additionally, if the fossil teeth are still mounted in the jaws, the whole crown is usually not accessible, and hence

–Š‡Š‡‹‰Š–‘ˆ–Š‡…”‘™…ƒ‘–„‡‡ƒ•—”‡†ȋ‡š…‡’–—•‹‰ƒ‹•ǯǦ”ƒ›‡–Š‘†ȌǤ

Figure 3: ‘••‹Ž‘ˆƒ”‹‰Š–—’’‡”•‡…‘†‘Žƒ”ǡ–”‹„‡Ž…‡Žƒ’Š‹‹Ǣ—”ƒƒ„ƒ•‹

‡›ƒǡˆ”‹…ƒǢ‘–‡‡„‡”ȋ͝Ǥ͢͡Ȃ͝Ǥͥ͟›ƒȌǤ

Phylogenies and fossils

A strong focus in the more recent years of macroevolutionary research has been the integration of fossils in the phylogenetic comparative analyses of

„‘–Š†‹˜‡”•‹Ƥ…ƒ–‹‘ƒ†–”ƒ‹–‡˜‘Ž—–‹‘ȋ”‡˜‹‡™‡†‹‡‡ŽŽƬƒ”‘͜͟͞͝Ǣ

—–Ƭƒ„‘•›͜͞͝͠Ǣ—–ƬŽƒ–‡”͜͢͞͝ȌǤ‡”‡™‘—Ž†Ž‹‡–‘ˆ‘…—•‘ƒˆ‡™

†‹ƥ…—Ž–‹‡•‡…‘—–‡”‡†™Š‡Ƥ†‹‰™ƒ›•–‘‹…Ž—†‡Š›’•‘†‘–›‹‘†‡Ž•

‘ˆ–”ƒ‹–‡˜‘Ž—–‹‘ƒ††‹˜‡”•‹Ƥ…ƒ–‹‘ǤŠƒ˜‡•–—„„‘”Ž›•–—…™‹–Š–Š‡†ƒ–ƒ•‡–

from Janis (1988), both out of necessity and in order to have a consistent

measurement of hypsodonty. This meant, as previously mentioned, that I could include only a limited number of extant ruminant species in the comparative analyses of Papers I and II.

To model hypsodonty evolution in Paper I, we focused on Ornstein- Uhlenbeck (OU) models, which require a tree with branch lengths scaled in units of time, as well as selective regimes mapped onto internal branches of a phylogeny, in addition to data on the tips. The selective regimes were

reconstructed with the use of ancestral niche reconstructions, based exclusively on extant data, in BEAST (Drummond et al. 2012). We corrected these

reconstructions based on the information from the fossil record of grassland.

This allowed us to compare the timing of hypsodonty evolution to the timeline of grassland evolution more directly than the common way of simply discussing the results in relation to the timing of events on the geological time scale.

In an ideal world, information from extant species and information on environmental constraints and temporal patterns should be used

simultaneously for estimations of ancestral niches. When it comes to including fossils in building phylogenies, not only as minimum age calibrations but

also their morphologies, one approach usually comes to mind. The approach

Šƒ•„‡‡”‡ˆ‡””‡†–‘ƒ•–Š‡Dz–‘–ƒŽ‡˜‹†‡…‡dzƒ’’”‘ƒ…ŠǢ‹–ƒ––‡’–•–‘…‘„‹‡

phylogenetics data from extant lineages (molecular, morphological) with data from extinct lineages (morphological) to build phylogenetic trees. However,

–Š‹•Šƒ•’”‘˜‡†‹ƥ…—Ž––‘ƒ’’Ž›‹ƒ—„‡”‘ˆ…ƒ•‡•ˆ‘””‡ƒ•‘••—…Šƒ•ǣ

†‹ơ‡”‡…‡•‹†‡Ƥ‹‰•’‡…‹‡•„‡–™‡‡‡š–‹…–ƒ†‡š–ƒ––ƒšƒǡ‹••—‡•‘ˆ

”ƒ†‘•ƒ’Ž‹‰‘ˆ–ƒšƒǡ‡–Š‘†‘Ž‘‰‹…ƒŽ…ŠƒŽŽ‡‰‡•‡–…Ǥȋ‡‡ŽŽƬƒ”‘

2013). There is an additional concern if we were to apply this approach to build a phylogenetic tree informed by ruminant fossils, to be used later in the analysis of morphological evolution. Namely, the morphological data used for the fossils often includes teeth morphologies, which could potentially render our analysis of evolution of hypsodonty circular. Furthermore, this would still only include the fossil record of the trait and not the environment, and would not inform the analysis about the timing of the spread and dominance of grasslands.

Accordingly, the way we included fossils in our models is not perfect, but I consider it a step in the right direction for merging knowledge from the fossil record in analyses of extant taxa.

There has been much research on how to estimate diversity in the face of an incomplete fossil record, and great progress has been made in terms of methodology (reviewed in Alroy 2010). However, in Paper II we apply the SSE methods that do not include fossils, but have the advantage of jointly

‘†‡ŽŽ‹‰–”ƒ‹–‡˜‘Ž—–‹‘ƒ††‹˜‡”•‹Ƥ…ƒ–‹‘ǤŠ‡”‡ƒ”‡ǡ‡˜‡”–Š‡Ž‡••ǡ…‘…‡”•

”‡‰ƒ”†‹‰–Š‡•‡‡–Š‘†••—…Šƒ•ǣ–Š‡†‹ƥ…—Ž–›‘ˆ‡•–‹ƒ–‹‰‡š–‹…–‹‘”ƒ–‡•ǡ

‘”†‡–‡…–‹‰†‹ơ‡”‹‰†‹˜‡”•‹Ƥ…ƒ–‹‘”ƒ–‡•„‡–™‡‡–”ƒ‹–•ǡˆƒŽ•‡Ž›Ž‹‹‰–”ƒ‹–•

–‘†‹ơ‡”‡–‹ƒŽ†‹˜‡”•‹Ƥ…ƒ–‹‘‡–…Ǥȋǯ‡ƒ”ƒƬ‡ƒ—Ž‹‡—͜͢͞͝ȌǤ††‹–‹‘ƒŽŽ›ǡ

–Š‡•’‡…‹Ƥ…‹••—‡•™‡‡…‘—–‡”‡†‹ƒ’‡””‡Žƒ–‡–‘•ƒ’Ž‹‰ƒ†ƒ…‡•–”ƒŽ

reconstruction, as well as estimates of extinction, which is the more general

‹••—‡‡–‹‘‡†ƒ„‘˜‡Ǥ™‘‘ˆ–Š‡‡–Š‘†•™‡‡’Ž‘›‡†ȋ ‹–œ‘Š͜͞͝͞Ǣ

‡ƒ—Ž‹‡—Ƭǯ‡ƒ”ƒ͜͢͞͝Ȍ”‡“—‹”‡–Š‡‹…Ž—•‹‘‘ˆƒƒ’’”‘š‹ƒ–‡•ƒ’Ž‹‰

rate at the tips, namely to what degree does our data include the known

entirety of the clade. Additionally, the third method (FitzJohn 2010) that uses categorical data requires the same sampling rate, but as sampling fractions for

‡ƒ…Š–”ƒ‹–…ƒ–‡‰‘”›‘ˆ–Š‡–”ƒ‹–ǤŠ‹•…‘—Ž†„‡“—‹–‡†‹ƥ…—Ž––‘‡•–‹ƒ–‡‹ˆ–Š‡”‡

‹•‘‹ˆ‘”ƒ–‹‘‘–Š‡•’‡…‹Ƥ…–”ƒ‹–•–ƒ–‡‘ˆ–ƒšƒ‹••‹‰‹‘—”’Š›Ž‘‰‡›Ǥ In regards to ancestral reconstruction, these methods have their own in-built algorithms for reconstructing traits back in time, so it was not straight-forward to, for example, include the corrected reconstructions we used in Paper I.

ƒ•–Ž›ǡ‘—”‡•–‹ƒ–‡•‘ˆ‡š–‹…–‹‘”ƒ–‡•™‡”‡‡š–”‡‡Ž›Ž‘™ǡƒ†Šƒ†‘‡ơ‡…–

‘†‹˜‡”•‹Ƥ…ƒ–‹‘”ƒ–‡•ǤŠ‹•‹•‘•–Ž‹‡Ž›‘–ƒ–”—‡”‡ƪ‡…–‹‘‘ˆ–Š‡Š‹•–‘”›

of this clade, but more of an artefact of the methods, given that the ruminant fossil record contains taxa that are extinct today. This is an example of how the fossil record could inform the results from analyses that use only extant taxa.

The papers

Paper I Millions of years behind: Slow adaptation of ruminants to

grasslands

This paper can be divided in two parts. One is an update of the phylogenetic relationships within Cetartiodactyla, a larger clade that ruminants make up the majority of. This work uses molecular data from mitochondrial DNA from Hassanin et al. (2012) with 16 new fossil calibration points, most of which (11) are within the ruminant clade. Additionally this new updated tree includes ancestral reconstructions of ruminant diet, habitat and geographic distribution. The second part concerns the analyses of trait evolution along the pruned tree of Cetartiodactyla to include only ruminants we had hypsodonty data on. The use of OU models of trait evolution lets us account for lag in adaptation, as well as allow for a more accurate phylogenetic correction based on residual correlations. Additionally, we used the aforementioned ancestral reconstructions and correct these with fossil information regarding the

timeline of the grassland evolution. This allowed us to account for not only the Ƥ”•–ƒ’’‡ƒ”ƒ…‡‘ˆ‰”ƒ••Žƒ†•ǡ„—–ƒŽ•‘–‘…‘’ƒ”‡–Š‹•–‘–Š‡–‹‡™Š‡–Š‡•‡

„‹‘‡•„‡…ƒ‡†‘‹ƒ–‘†‹ơ‡”‡–…‘–‹‡–•ǡ™Š‹…Š‹•’‡”Šƒ’•™Š‡–Š‡›

™‡”‡‘•–—–‹Ž‹œ‡†„›”—‹ƒ–•Ǥ‡ƒ††–‘–Š‡†‡„ƒ–‡‘ˆ–Š‡‹ƪ—‡…‡‘ˆ†‹‡–

˜‡”•—•Šƒ„‹–ƒ–‘–Š‡‡˜‘Ž—–‹‘‘ˆŠ›’•‘†‘–›„›ƒƥ”‹‰–Šƒ––Š‡›’Žƒ›‡†

ƒŽ‘•–‡“—ƒŽ”‘Ž‡•‹–Š‹•ƒ†ƒ’–ƒ–‹‘ǡ„—––Šƒ––Š‡‹”Œ‘‹–‡ơ‡…–•Šƒ†–Š‡‘•–

•‹‰‹Ƥ…ƒ–‹ƪ—‡…‡Ǥ ‘ŽŽ‘™‹‰–Š‡•‡”‡•—Ž–•™‡‡…‘—”ƒ‰‡ƒ‘”‡‹…Ž—•‹˜‡

analysis of these variables when investigating hypsodonty. This study is an attempt to more directly include grass fossils and the history of grasslands in the analysis of hypsodonty evolution, which is a crucial step since the two are tightly intertwined and a part of a textbook example of macroevolution and adaptation.

3DSHU,,:KRLVELWLQJWKHGXVW"'HQWLWLRQ²GHSHQGHQWGLYHUVLÀFDWLRQ dynamics in ruminants

‘”’Š‘Ž‘‰‹…ƒŽ–”ƒ‹–•Šƒ˜‡Ž‘‰„‡‡—•‡†–‘—†‡”•–ƒ††‹˜‡”•‹Ƥ…ƒ–‹‘

patterns, and ruminant hypsodonty is no exception. This diverse clade has been

‹˜‡•–‹‰ƒ–‡†–‘†‡–‡”‹‡–Š‡‹ƪ—‡…‡–Šƒ––Š‡‹”†‹‡–ǡ„‹‘‹…•’‡…‹ƒŽ‹œƒ–‹‘

and hypsodonty had on speciation and extinction dynamics (Cantalapiedra

͜͞͝͝ǡ͜͞͝͠Ǣƒ‹ƒ‡–ƒŽǤ͜͞͝͝ȌǤ–Š‹•’ƒ’‡”ǡ™‡’”‡•‡––Š‡Ƥ”•–Œ‘‹–ƒƒŽ›•‹•‘ˆ

Š›’•‘†‘–›‡˜‘Ž—–‹‘ƒ†’ƒ––‡”•‘ˆ†‹˜‡”•‹Ƥ…ƒ–‹‘‹–Š‹•‰”‘—’Ǥ‡—•‡

a set of recently developed phylogenetic comparative methods (Maddison

‡–ƒŽǤͣ͜͜͞Ǣ ‹–œ‘Š͜͜͞͝ǡ͜͞͝͞Ǣ‡ƒ—Ž‹‡—Ƭǯ‡ƒ”ƒ͜͢͞͝Ȍǡ™Š‹…ŠƒŽŽ‘™ˆ‘”

–Š‡‡˜‘Ž—–‹‘‘ˆƒ–”ƒ‹––‘‹ƪ—‡…‡ƒ†‹–—”„‡‹ƪ—‡…‡†„›–Š‡”ƒ–‡•‘ˆ

speciation and extinction. Furthermore these methods can distinguish between

’ƒ––‡”•‘ˆ™‹–Š‹Ž‹‡ƒ‰‡†‹˜‡”•‹Ƥ…ƒ–‹‘ƒ•‘’’‘•‡†–‘–Š‡•‡†›ƒ‹…•„‡‹‰

†”‹˜‡„›–Š‡–”ƒ•‹–‹‘•‹–”ƒ‹–•–ƒ–‡•ȋ‹Ǥ‡Ǥƒƒ‰‡‡•‹•ȌǤ‡Ƥ†Š‹‰Š•’‡…‹ƒ–‹‘

rates in species with high-crowned teeth, meso- and hypsodont teeth (the two

‹††Ž‡…ƒ–‡‰‘”‹‡•‘—–‘ˆˆ‘—”Ȍǡƒ†ƒ‡‰Ž‹‰‹„Ž‡‹ƪ—‡…‡‘ˆ–Š‡‡š–‹…–‹‘”ƒ–‡•

‘–Š‡’ƒ––‡”‘ˆ”—‹ƒ–†‹˜‡”•‹Ƥ…ƒ–‹‘ǤŠ‡Žƒ––‡”‹•‘•–Ž‹‡Ž›ƒƒ”–‡ˆƒ…– of the methodology and is discussed in Paper II. In addition, we discover an

‹ƪ—‡…‡‘ˆƒ–Ž‡ƒ•–‘‡‘–Š‡”ǡŠ‹††‡˜ƒ”‹ƒ„Ž‡ǡ‘–Š‡‹…”‡ƒ•‡†•’‡…‹ƒ–‹‘

”ƒ–‡•ǤŠ‹••–—†›ƒ††•–‘–Š‡†‹•…—••‹‘‘ˆ”—‹ƒ–†‹˜‡”•‹Ƥ…ƒ–‹‘„›•–”‡••‹‰

the importance of hypsodonty, as well as the need to investigate other potential causes of the present-day patterns. It also adds information on broader

evolutionary questions about the connection between phenotypic adaptive traits and present-day biodiversity.

3DSHU,,,)RVVLOERYLGWHHWKUHFRUGUHÁHFWVSRODUL]HGGLHWWKURXJKRXW the Late Neogene of Africa

This study focuses on a diverse group within the ruminant clade – African bovids, which represent the majority of present-day ruminants. African bovids are an excellent example of an array of molar-crown morphologies, and are hence an interesting group on which to test questions of dental evolution.

Bovids have historically been divided by systematists into tribes--a taxonomic group above a genus level and below family and subfamily level--according

–‘‘”’Š‘Ž‘‰‹…ƒŽǡ’Š›•‹‘Ž‘‰‹…ƒŽǡƒ†„‡Šƒ˜‹‘”ƒŽ–”ƒ‹–†‹ơ‡”‡…‡•„‡–™‡‡–Š‡

–”‹„‡•Ǥ–Š‹••–—†›ǡ™‡†‡˜‹•‡ƒ‡™•…‘”‹‰•›•–‡‘ˆ–‘‘–Š…”‘™••’‡…‹Ƥ…ƒŽŽ›

–ƒ‹Ž‘”‡†–‘…ƒ’–—”‡•—„–Ž‡†‹ơ‡”‡…‡•„‡–™‡‡–Š‡–”‹„‡•ǡ™Š‹…Š…‘—Ž†„‡ƒ‡›

in disentangling their dietary adaptations. We focus on traits related to the

•Šƒ’‡‘ˆ–Š‡…Š‡™‹‰•—”ˆƒ…‡ƒ†•–”—…–—”ƒŽˆ‘”–‹Ƥ…ƒ–‹‘•‘ˆ–Š‡…”‘™ǡ™Š‹…Š

Šƒ˜‡–Š‡’‘–‡–‹ƒŽ–‘‹ƪ—‡…‡ˆ‘‘†’”‘…‡••‹‰Ǥ‡—•‡–™‘†‹ơ‡”‡–…Ž—•–‡”‹‰

methods to answer the question of whether bovids group taxonomically or morphologically. Meaning: are the groups within bovids a consequence of the shared history and/or tribal characteristics, or are they formed as a result

‘ˆ†‡–ƒŽ‘”’Š‘Ž‘‰‹‡••—‹–‡†–‘†‹ơ‡”‡–‹ƒŽ†‹‡–ƒ†Šƒ„‹–ƒ–’”‡ˆ‡”‡…‡•ǫ

††‹–‹‘ƒŽŽ›™‡–‡•–ˆ‘”–Š‡‹ƪ—‡…‡‘ˆ’ƒ•–…Ž‹ƒ–‡ǡ•’‡…‹Ƥ…ƒŽŽ›–‡’‡”ƒ–—”‡

and precipitation, on the resulting clusters, in order to investigate whether dental adaptations are related to habitat characteristics. Lastly, we use the clusters resulting from the morphological analyses to see how well they can predict past climate, since mammalian fossil taxa and their morphologies

ƒ”‡‘ˆ–‡—•‡†ƒ•‹†‹…ƒ–‘”•‘ˆ’ƒ•–‡˜‹”‘‡–•Ǥ‡Ƥ†–Šƒ–„‘˜‹†•ˆ‘”

–™‘…Ž—•–‡”•†”‹˜‡„›†‹ơ‡”‡…‡•‹–‘‘–Š‘”’Š‘Ž‘‰‹‡•ǡ‘•–Ž‹‡Ž›†—‡–‘

the split between browsers and grazers. We also note that this split possibly occurred as early as 7 million years ago when the earliest bovids were appearing in Africa. Furthermore, tooth-crown morphologies seem to be a good predictor of both past precipitation and geological age. Our hope is that this study adds to data on bovid dental evolution, as well as to broader research on the past biodiversity and climate of the African continent.

Concluding remarks and future perspectives

It was humbling to work on ruminants, a system that has received much attention over several decades, and where a lot of research has

already been done on the importance of morphological traits in relation to

ƒ…”‘‡˜‘Ž—–‹‘ƒ”›’ƒ––‡”•Ǥ—‹ƒ–•ƒ”‡Œ—•–‘‡‘—–‘ˆƒ›‰”‘—’•‘ˆ

mammals that have seized the attention of paleobiologists, and, more broadly, evolutionary biologists, as a part of a story of the evolution of herbivores over million-year long timescales. Perhaps the most famous part of this story is the evolution of the horse, a close relative of ruminants, which became a common component of evolutionary biology textbooks. Despite decades of research, the evolutionary tempo and mode, as well as certain aspects of the impact of various determinants on the evolution of hypsodonty, remain murky. My goal was to further disentangle standing debates and add new information to research on ruminant dental evolution, using rigorous quantitative methods and new data.

—‹ƒ–•ƒ”‡‘‡‘ˆ–Š‡‘•–†‹˜‡”•‡‰”‘—’•‘ˆŽƒ”‰‡–‡””‡•–”‹ƒŽƒƒŽ•

today, and their radiation is tightly linked to climate and ecological changes.

In addition to contributing to debates on ruminant dental evolution and key adaptations, this dissertation more broadly highlights the importance of

examining trait evolution with the use of appropriate models that can account for temporal lags in adaptation. By recovering such a lag in the evolution of

Š›’•‘†‘–›ǡ–Š‹•™‘”ƒŽ•‘ƒ††•–‘Ƥ†‹‰•‘ˆ•Ž‘™ƒ†ƒ’–ƒ–‹‘‘ˆ’Š‡‘–›’‹…

traits on long time scales (Uyeda et al. 2011). In order to elucidate this

convoluted story, it was necessary to include not only the temporal pattern of hypsodonty evolution, but also the timing of the biotic shifts in grassland

‡˜‘Ž—–‹‘‘†‹ơ‡”‡–…‘–‹‡–•ȋƒ’‡”ȌǤŽ›™Š‡™‡‹…Ž—†‡„‘–Š’ƒ•–

and present environmental context in our analyses of trait evolution will we get a more holistic story of macroevolutionary trends.

‘•–’ƒ•–”‡•‡ƒ”…Š‘’ƒ––‡”•‘ˆ†‹˜‡”•‹Ƥ…ƒ–‹‘™ƒ•†‘‡™‹–Š‘—–

the inclusion of trait evolution. We show through the adaptive nature

‘ˆŠ›’•‘†‘–›–Šƒ–‹–‹•Ž‹‡Ž›–Šƒ–•—…Šƒ–”ƒ‹–™‘—Ž†‹ƪ—‡…‡”—‹ƒ–

†‹˜‡”•‹Ƥ…ƒ–‹‘Ǥ‡…‡–Ž›†‡˜‡Ž‘’‡†‡–Š‘†•–Šƒ–Œ‘‹–Ž›ƒ††”‡••–Š‡‡˜‘Ž—–‹‘

‘ˆƒ–”ƒ‹–ƒ††‹˜‡”•‹Ƥ…ƒ–‹‘’ƒ––‡”•‘ˆ–Š‡…Žƒ†‡‘ˆ‹–‡”‡•–ƒŽŽ‘™‡†—•–‘–‡•–

this (Paper II). Interestingly, we found increased rates of speciation in taxa in the middle of the hypsodonty spectrum (meso- and hypsodont), which were not the consequence of higher transition rates towards higher hypsodonty

˜ƒŽ—‡•ǤŠ‹•’‡”Šƒ’•’‘‹–•–‘–Š‡†‹ƥ…—Ž–‹‡•‘ˆ†‡˜‡Ž‘’‹‰ƒ†Ȁ‘”ƒ‹–ƒ‹‹‰

high levels of hypsodonty, so future work on genetic and developmental basis of

Š›’•‘†‘–›…‘—Ž†•Š‡†‘”‡Ž‹‰Š–‘–Š‹•Ǣ‹ˆ–Š‡”‡ƒ”‡…‘•–”ƒ‹–•‹˜‘Ž˜‡†ǡ–Š‹•

could explain the lag we recover in Paper I.

•’”‡˜‹‘—•Ž›†‹•…—••‡†ǡŠ›’•‘†‘–›‹†‡š‹•ƒ†‹ƥ…—Ž––”ƒ‹––‘ƒ…“—‹”‡

and measure in the fossil record. In addition to this, it is a simple ratio of two linear measurements, which might not capture the complexity of teeth-crown morphologies important for food processing. Hence, in Paper III we developed alternative ways of scoring mammal teeth that are particularly adapted to

characterizing bovid teeth. We show the importance of tooth morphology

ˆ‘”†‹‡–ƒ”›ƒ†ƒ’–ƒ–‹‘•ƒ†…‘Ƥ”‹–•—–‹Ž‹–›‹’”‡†‹…–‹‰’ƒ•–…Ž‹ƒ–‡

…‘†‹–‹‘•ǤŠ‡•‡‡™‡ƒ•—”‡‡–•…‘—Ž†„‡—•‡†ƒ•ƒ’”‘š›ˆ‘”†‹ơ‡”‡–

paleoenvironments and climates in order to circumvent the use of hypsodonty which is tied to existence of a time lag in adaptation. Additionally, we highlight the potential that 3D data and methodology could have in addressing the

hypotheses of dental evolution and adaptation.

It is my belief that by re-examining old questions with new data and improved methods, we can gain new perspectives and be surprised by the

”‡•—Ž–•Ǥ›Š‘’‡‹•–Šƒ–ǡƒ•‡–Š‘†‘Ž‘‰‹…ƒŽ†‡˜‡Ž‘’‡–•ƪ‘—”‹•Šǡ™‡‡‡’‹

mind the underlying biological processes and aim for overarching approaches to answer questions regarding macroevolution. I think part of this will be to always keep in mind that although fossils represent the past, they might also hold the key to the future.

Acknowledgements

Šƒ•–‘ ƒ„”‹…‡”‘—Šƒ‘ơǡŠ‘ƒ• Ǥƒ•‡ǡ‡‡•‹ƒ‰‹‘™ǡ

Katie Owers, Cassandra Trier and Kjetil L. Voje for helpful comments on the

‹–”‘†—…–‹‘ǡƒ•™‡ŽŽƒ•ƒƒœœƒ”‡ŽŽƒˆ‘”Žƒ›‘—–‡†‹–‹‰ǤŠƒ›‘—–‘ƒ›

Troll for generously sharing his artwork and allowing the print of the image in the Preface. Figure 2. is reprinted with permission from Cambridge University Press. Paper I is reprinted with permission from the publisher.

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”—‹ƒ–•Ǥ‹‘ŽǤ‡˜Ǥͤ͜ǣͥ͢͞Ȃ͟͜͞Ǥ

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