From local adaptation to range sizes
Alzate Vallejo, Adriana
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Alzate Vallejo, A. (2018). From local adaptation to range sizes: Ecological and evolutionary consequences of dispersal. Rijksuniversiteit Groningen.
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SUMMARY
Why do some species occupy almost all of the Earth’s terrestrial (e.g. barn owl) or marine (e.g. moon fishes) systems, whereas others are only found in single fresh-water springs (like the devil‘s hole pupfish) or on small, isolated islands?. What is impeding species to occupy all of the Earth? Is it that species cannot reach all places because of reduced dispersal abilities? Or is it that geometric constraints and habitat availability plays an important role on how far species can go? Is it that species are adapted to certain abiotic conditions (e.g. salinity, temperature, etc) and they are unable to adapt to habitats where conditions are different? Or is it that they cannot successfully colonize habitats in which competitor species are already present? Is it that just given enough time all species will be able to occupy all places, so older species are more widespread than younger ones?
Ultimately, only a few processes are important in determining a species’ range size: speciation (creation/division of ranges) dispersal to a new habitat (expan-sion of the range), successful colonization of that habitat (successful dispersal) and (avoidance of) local extinctions. Among these processes, dispersal has a central role as it is important for population’ persistence in suboptimal habitats, by providing demographic rescue to populations that otherwise would go extinct. Furthermore, dispersal also promotes gene flow, bringing the genetic variability necessary for ad-aptation, which is important for successful colonization and ultimately range expan-sion. In this thesis, using a wide variety of approaches and model systems, I study how these various mechanisms can act together to eventually determine range sizes.
Firstly, I used two evolutionary experiments (with spider mites) to investigate how dispersal drives local adaptation and survival of organisms to a new habitat, and how the effects of dispersal are mediated by habitat size and by the competition with a locally co-occurring species. Secondly, I used a process-based model in which I in-corporate all processes affecting geographical species ranges (dispersal, speciation, birth-death dynamics) to explain the emergence of the empirical patterns of range size distributions of reef fishes. Thirdly, I used a correlational study to explore how important dispersal is compared to other factors in driving range size in reef fishes.
The two experimental studies showed that dispersal (of immigrans that are not adapted to the local conditions) exerts both positive and negative effects on colo-nization, extinction and local adaptation. Positive effects occur, even though most immigrants might not be well adapted to the new conditions, when by chance some of the immigrants might bring alleles that confer an advantage to the individual to cope with the new local conditions, thus spreading these advantageous alleles to the
island population. Negative effects occur when too high levels of dispersal will bring too many non-adapted individuals that by reproducing with the local population (which is adapted or in the process of adaptation) will swamp the adaptation of the local population, thus hindering adaptation (migration load). The relationship bet-ween dispersal and adaptation can be described as a bell-shaped relationship, with an optimum at intermediate levels of dispersal.
Besides dispersal, there are many other factors that can affect colonization-ex-tinction dynamics and adaptation, and thus affect range expansion. Firstly, because the ideal habitat for a certain species is never homogeneously distributed (neither spatially nor temporary), the spatial configuration of the habitat (islands, reefs, patches of forest) can play an important role. Some of the first recognizing the im-portance of geographical features on biodiversity were MacArthur and Wilson in their Island Biogeography Theory (IBT).Thus island size and isolation from a main-land (that can be translated in differences in dispersal) can drive biodiversity, ad-aptation and speciation via colonization-extinction dynamics. Although the effects of colonization and extinction on species richness were already demonstrated by many other theoretical, empirical and experimental studies, the role of evolution in island biogeography has never been experimentally tested before. Using experimen-tal biogeography, I confirmed that dispersal increases colonization success and that island size affects extinction. More importantly, I showed how the same factors that influence extinction and colonization can affect local adaptation. The smaller the habitat and the closer the habitat to the mainland (thus more immigration), the less likely adaptation occurrs.
Not only physical or abiotic factors, but also biotic factors can affect the suc-cess of a population in colonizing and adapting to a new habitat, and consequently in expanding its range. For example, interspecific competition can reduce popula-tion size and increase extincpopula-tion risk, because stochastic demographic fluctuapopula-tions are likely to affect smaller populations more than larger ones. Using experimental evolution, I showed that strong competition can lead to unsuccessful colonization, low population sizes and high extinction risk. Competition will therefore negatively impact range expansion, as these island populations do not have a chance to adapt to the local habitat. However, I observed that competition can be beneficial in some circumstances. When populations are receiving a large influx of immigrants, which otherwise will negatively impact adaptation (via genetic load), competition allows adaptation by purging the population of most of the maladapted immigrants. As the realized immigration is lower and selection is stronger, this allows for the benefits of dispersal on local adaptation.
With the first two experimental studies on spider mites (chapters 2 and 3), I illustrated several mechanisms through which dispersal can affect range expansion.
However, to understand how important these mechanisms are in the real world, ob-servational studies jointly examining how dispersal and other factors drive species range sizes might provide a more complete picture. Using a spatially explicit neutral model (chapter 4), I showed that species range size distributions in reef fishes can be explained by a combination of stochastic birth, death, speciation and variable dispersal abilities. In a scenario with strong dispersal limitation a large proportion of the species of the metacommunity attained small ranges and very few occupied the complete region. In contrast, in a scenario of low dispersal limitation, most of the species attained very large range sizes. I confirmed the positive effect of dispersal on range size by using a correlational study (chapter 5), which shows that range size is positively correlated with traits that are related to dispersal ability in reef fishes. Fishes that have pelagic eggs, high adult mobility and have large body size attain larger range sizes than fishes that have non-pelagic eggs and low adult mobility and are smaller.
To summarize, in this thesis I investigated the role of dispersal in driving ad-aptation to new habitats and ultimately, range sizes. Although it is clear that disper-sal is a key trait (or set of traits) that strongly affects the ability of species to reach new habitats, to locally adapt and to obtain large range sizes, there is still a lot that we do not understand. For example, within species with similar dispersal abilities, there is still a large variation of geographical ranges, which might be more related to differences in adaptation and to the community context (e.g. biological interac-tions). Understanding what drives the ability of species to adapt and maintain large ranges is one of the greatest scientific challenges and it is not only of fundamental interest, but also of high applied value. Range size is one of the strongest predictors of extinction rates, so explaining what drives range sizes will also help explaining what drives species’ vulnerability to extinctions. Furthermore, ongoing global chan-ges such as habitat loss and climate change will likely not only affect the need, but also the ability of species to adapt to novel environments.
NEDERLANDSE SAMENVATTING
Weinig soorten komen op Aarde overal voor. De kerkuil en maanvis zijn notoire uitzonderingen met een kosmopolitische verspreiding op land of in de oceanen. An-dere soorten komen echter enkel voor in één zeer lokale zoetwaterbron, of op kleine sterk geïsoleerde eilanden. Wat beperkt hun verspreiding? Kan het zijn dat deze soorten over zo’n geringe mobiliteit beschikken dat ze nergens anders geraken? Of wordt hun verspreiding vooral bepaald door landschappelijke factoren en de bes-chikbaarheid van habitat? Of kunnen soorten zich gewoonweg niet aanpassen aan andere omgevingsomstandigheden? Of zijn het net andere soorten die hun verspre-iding belemmeren? Misschien is het wel zo dat veel soorten evolutionair zo jong zijn dat ze de tijd nog niet hebben gehad om zich te verspreiden?
Volgens de huidige inzichten bepalen slechts enkele ecologische factoren de grootte van de verspreidingsgebieden -de arealen- van soorten: speciatie of soort-vorming (leidend tot nieuwe arealen of de opsplitsing van een gemeenschappelijk areaal), dispersie of verbreiding (expansie van het areaal) en extinctie of uitster-ven (inkrimping van een areaal). Het dispersievermogen van soorten speelt hierbij steeds een centrale rol. Het laat bijvoorbeeld toe dat soorten kunnen overleven in marginaal habitat (putpopulaties) door de toevoer van nieuwe individuen uit bron-populaties. Dispersie zorgt echter niet alleen voor demografische fluxen, het zorgt ook voor de verspreiding van genen en de opbouw van de nodige genetische variatie om evolutionaire aanpassingen te mogelijk te maken. Deze evolutionaire dynamiek-en zulldynamiek-en dan finaal sterk terugkoppeldynamiek-en op de mogelijke expansie van het areaal. Ik bestudeerde de manier waarop deze processen samen arealen vormen door de integratie van experimenten aan de hand van modelorganismen (proces-gebaseerd) en diverse modelleertechnieken (patroon-georiënteerd).
Ik maakte gebruik van experimentele evolutie aan de hand van spintmijten om de na te gaan op welke manier dispersie de mogelijkheden van lokale adaptatie aan nieuwe omgevingscondities beïnvloedt, en hoe dit proces afhangt van de grootte van de leefgebieden en de aanwezigheid van concurrerende soorten. Daarnaast bouwde ik de mechanismen van dispersie, speciatie en demografie in mechanistische mod-ellen in die me toelieten om de gekende verspreidingspatronen van koraalvissen te verklaren. Aan de hand van correlatieve modellen bepaalde ik finaal in welke mate dispersie dan wel andere soortkenmerken de huidige waargenomen arealen van ko-raalvissen best konden verklaren.
Mijn experimentele studies toonden aan dat de hoeveelheid immigranten die niet aangepast zijn aan de nieuwe omgevingscondities zowel een positieve als
negatieve impact kan hebben op de vestiging en kans op uitsterven, maar ook op de sterkte en snelheid van de genetische aanpassingen (lokale adaptatie). Positieve ef-fecten zijn het gevolg van de toevallige inbreng van genen die een selectief voordeel hebben onder de nieuwe omstandigheden. Wanneer door systematisch hoge dis-persie echter teveel niet-aangepaste immigranten zich vestigen zullen deze ervoor zorgen dat de voordelige genen zich niet kunnen verspreiden (de adaptaties ver-drinken in figuurlijke zin). De combinatie van beide mechanismen resulteert dan in een parabolisch verband tussen dispersie en adaptatie, waarbij adaptatie maximaal is wanneer de influx van nieuwe individuen niet te laag of te hoog is.
De dispersiecapaciteit van soorten zal echter sterk bepaald worden door de ruimtelijke spreiding van het habitat. Het belang van geografische factoren voor pa-tronen in soortenrijkdom werd vastgelegd in de biogeografische eilandtheorie van Mac Arthur & Wilson. Volgens deze theorie zal de isolatie van eilanden direct de immigratiekans van soorten bepalen, en dus ook de opbouw van soorten-diversiteit via demografische (kolonisatie-uitstervingsbalans) en evolutionaire processen (ad-aptatie en soortvorming). Alhoewel het belang van deze theorie reeds werd aange-toond voor patronen van soortenrijkdom, bestond er nog geen formele experiment-ele test omtrent haar belang voor evolutionaire dynamieken. Door gebruik te maken van experimentele evolutie binnen een kader van biogeografie (vasteland-eiland systeem) kon ik de hypothese dat isolatie en eilandgrootte de mate van adaptatie bepalen, aantonen.
Ook biotische interacties beïnvloeden de kolonisatiekansen en adaptieve pro-cessen aan nieuwe omgevingscondities. Ze zullen bijgevolg een grote invloed heb-ben op areaaluitbreidingen. Competitie met andere soorten kan bijvoorbeeld een rem zetten op de populatiegroei en daardoor de kans op lokaal uitsterven vergroten omdat stochastische demografische schommelingen nu eenmaal een hogere kans hebben te leiden tot extinctie wanneer populatiegroottes laag zijn. Ik kon dit aanto-nen aan de hand van experimentele evolutie. Omdat competitie daarom leidt tot een verlaging van de adaptieve capaciteiten zal ze iedere areaaluitbreiding vertragen of tegengaan. Ik observeerde echter ook dat competitie voordelig kan zijn: bij een hoge immigratie van niet-aangepaste individuen zal de anders negatieve impact op adap-tatie (zie hoger) net teniet gedaan worden. Omdat selectie verhoogt en de effectieve vestiging verlaagt wordt de verspreiding van de niet-voordelige genen verhinderd.
Aan de hand van experimenteel werk waarbij ik spintmijten als model gebruikte kon ik dus aantonen dat dispersie kan leiden tot de uitbreiding van arealen door de effectieve kolonisatie van habitats die qua omgevingsomstandigheden grondig ver-schillen van deze in het oorspronkelijk areaal (hoofdstukken 2,3). Om te begrijpen of deze factoren ook waargenomen patronen in de natuur verklaren ontwikkelde ik een modelmatige en patroongerichte aanpak. Door in eerste instantie gebruik te
maken van een ruimtelijk expliciet neutraal model (hoofdstuk 4), kon ik aantonen dat de gerealiseerde arealen van koraalvissen best verklaard konden worden door een combinatie van stochastische demografische processen, speciatie en variatie in dispersiemogelijkheden. Wanneer dispersie sterk gelimiteerd is, zal een groot deel van de soorten uit de metagemeenschap een klein areaal bezetten, terwijl slechts een minderheid van de soorten een echte globale verspreiding kunnen innemen. Wan-neer alle soorten over een heel groot verspreidingsvermogen beschikken werd een logisch omgekeerd patroon waargenomen. Deze theoretische voorspelling kon ik hard maken aan de hand van een correlatieve studie (hoofdstuk 5), waaruit bleek dat de grootte van de arealen bij koraalvissen positief geassocieerd was met kenmerken die op een goed verbreidingsvermogen duiden: pelagische eieren, een hoge adulte mobiliteit en een hoge lichaamsgrootte.
Ik bestudeerde dus het belang van dispersie voor genetische aanpassingen aan nieuwe omgevingen en haar effect op arealen. Alhoewel uit mijn onderzoek volgt dat dispersie hierbij een centraal proces is, blijkt tevens dat er nog grote kennis-lacunes zijn. Zo is de grote variatie in areaal tussen soorten met een vergelijkbare dispersiecapaciteit mogelijks het gevolg van verschillen in gemeenschapssamenstel-ling en dus biotische interacties. Het verkrijgen van inzichten in de mechanismen die soorten toelaten zich aan te passen aan veranderende omgevingen en daarbij dus hun verspreiding te maximaliseren is niet alleen een prangende vraag vanuit een fundamenteel academisch, maar zeker ook vanuit een toegepast perspectief. Aangezien de areaalgrootte het best de overlevingsmogelijkheden van soorten kan voorspellen, zullen inzichten die ons toelaten processen van areaalveranderingen te begrijpen finaal gebruikt kunnen worden om de uitstervingskansen en dus kwets-baarheid van soorten in te schatten. Uit mijn onderzoek bleek immers niet alleen dat globale veranderingen zoals klimaatsverandering en habitatfragmentatie niet enkel de noodzaak, maar ook de effectiviteit van evolutionaire aanpassingen aan nieuwe omgevingen bepalen.
ACKNOWLEDGMENTS
I would like to thank here to the people, researchers, institutions that (directly or indirectly) made the conclusion of this thesis possible.
My first two years I was hosted by the Terrestrial Ecology Unit (TEREC) of Ghent University. I would like to thank my colleagues there that made (scientif-ic) life much more enjoyable: Katrien, Jeroen, Steven, Jasmin, Laurence, Hans, Alexandre, Irene, Alejandro, Eduardo and Karen. I also want to thank to Angelica Alcantara for her continuous efforts to solve all my administrative problems. I thank Hans, Viki and Pieter for their technical assistance. I would like to thank Karen Bisschop (at that time a master student) and Jelle van den Bergh for the amount of effort they put into the evolutionary experiments, for taking care of the spider mites (they really spoilt them) and the tomato plants (up to the point that they developed tomato allergies!). Without their work chapters 2 and 3 would not have been possible. I also thank to Pieter de Pauw for making life outside the university possible.
My last two years (which turned out to be three) I was hosted by the Theo-retical Research in Evolutionary Life Sciences group (TRÊS) from the University of Groningen. I would like to thank my colleagues for amenable discussions (sci-entific or not): Cyrus, Liang, Leonel, Paul, Karen, Pancho, Joss, Kasper, Hanno and Richel. Thanks as well to Ingeborg Jansen, which is always keen to help with a smile on her face. I especially would like to thank Corine Eising for helping me out so many times I can’t even remember.
I already had a long history with life in Groningen, so my thanks go back to past times. I would like to thank the 2009 cohort of the top master program in evolution-ary biology: Andres, Hernan, Jordi, Lotte, Alex, Rienk, Froukje and Michiel. I like to thank all Dutch people during the course period, for a 6 month (or even longer) immersion course into the Dutch culture of single-ingredient sandwiches and the use of weather apps. My special thanks go to Jordi for showing (or pretending to show) interest in my innumerable non-sense ideas. I also thank Andres and Hernan for making feel Groningen a bit more like home. Also thank to Linda and Jelle for the extra Dutch and Frisian culture lessons.
I would also like to thank many people for making the last few months of my PhD studies, which I spent in Leipzig, more enjoyable. My thanks go to Roel, Corin-na, Camilo and Julius (thanks for teaching me how to use photoshop and a pad for making the cover of this thesis!). I would also like to thank Jonathan Chase for or-ganizing a workspace for me at iDiv.
scientific thesis.
Thanks to the people that were directly involve in my research: my coauthors. I thank Thijs Janzen, Fons van der Plas, Karen Bisschop, Fernando A. Zapata, James Rosindell, Dries Bonte and Rampal Etienne. I especially thank James Rosindell for his effort, his hours of mentoring and long skype meetings and discussions that help the realization of chapter 4. Most importantly, I would like to thank my supervisors: Dries and Rampal. Dries for being always available for either a quick question or long discussions and in addition for translating my summary to Dutch. Thanks to Rampal for encouraging me to apply for the top master program in Evo-lutionary Biology one week before the deadline! Also, thanks for offering me solu-tions and help when I needed it (like when he offered me the PhD position) and for the innumerable useful discussions.
I also would like to thank my parents (Mariela and Manuel), as they are the ultimate cause of this thesis. Thanks to my brother (Juan Manuel) for… being my brother ;). I also would like to thank my adoptive family (Liesbeth, Kees, Ruben, Irene, Maarten and OmaOma) for welcoming me and making me feel at home.
Finally, I would like to thank Fons and Fiona for making life happier and more exciting!
PUBLICATIONS
1. Alzate, A., Etienne, R. S. & Bonte, D. Experimental island biogeography demonstrates the importance of island size and dispersal for the adaptation to novel habitats. In press. Global Ecology and Biogeography. DOI: 10.1111/ geb.12846
2. Alzate, A., Janzen, T., Bonte, D., Rosindell, J. & Etienne, R. S. A simple spa-tially explicit neutral model explains range size distributions of reef fishes. Global Ecology and Biogeography. Under review. (also on bioRxiv, 238600, DOI: 10.1101/238600)
3. Alzate, A., van der Plas, F., Zapata, F.A., Bonte, D., & Etienne, R. S. Incom-plete datasets obscure correlations between traits related to dispersal and ge-ographic range size of reef fishes in the Tropical Eastern Pacific. Ecology and Evolution. Under review.
4. Alzate, A., Bisschop, K., Etienne, R. S. & Bonte, D. 2017. Interspecific compe-tition counteracts negative effects of dispersal on adaptation of an arthropod herbivore to a new host. Journal of Evolutionary Biology. 30(11):1966-1977. 5. Janzen, T., Alzate, A., Muschick, M., Maan, M. E., van der Plas, F. & Etienne,
R. S. 2017. Community assembly in Lake Tanganyika cichlid fish: quantify-ing the contribution of both niche-based and neutral processes. Ecology and Evolution. 7(4): 1057-1067.
CURRICULUM VITAE
Adriana Alzate Vallejo was born on the 25th of Au-gust 1982 in Cali, Colombia. She studied Biology at Universidad del Valle (Cali, Colombia), finishing her bachelor with emphasis on Ecology in 2005. In 2009 she was awarded a talent grant to follow the
Topmas-ter Program in Evolutionary Biology at the University of Groningen, the Neth-erlands. She obtained her master’s degree in Ecology and Evolution in 2011. She started a joint PhD program from the Universities of Groningen and Ghent in 2013. Currently, she is part of the Adaptation and Evolution Research Group of the German Center for Integrative Biodiversity Research (iDiv) Halle-Je-na-Leipzig, in Leipzig, Germany.
6. Kölzsch, A., Alzate, A., Bartumeus, F., de Jager, M., Weerman, E., Hengeveld, G.M., Naguib, M., Nolet, B.A. & van de Koppel, J. 2015. Experimental evi-dence for inherent Lévy search behaviour in foranging animals. Proceedings of the Royal Society B. 282(1807): 20150424.
7. Alzate, A., Zapata, F. A. & Giraldo, A. 2014. A comparison of visual and col-lection-based methods for assessing community structure of coral reef fishes in the Tropical Eastern Pacific. Revista de Biologia Tropical. 62: 359-371. 8. Alzate, A., Muñoz, G. G., Zapata, F. A. & Giraldo, A. 2012. New records of
cryptobenthic fishes in coral reef habitats of Gorgona island, Colombia, Trop-ical Eastern Pacific. Bulletin of Marine and Coastal Research. 41: 229-235. 9. Alzate, A. & F. A. Zapata. 2007. Estructura de la comunidad de peces en dos
formaciones coralinas de Isla Malpelo: 98-104. In: INVEMAR. 2007. Informe del estado de los ambientes marinos y costeros en Colombia: Año 2006. Serie de publicaciones periódicas Nº 8. Santa Marta, 378 p.
10. Alzate, A. & F. A. Zapata. 2007. Estructura de la comunidad de peces de ar-recifes rocosos en ambientes marinos y estuarinos del Pacífico: 191-195. In: INVEMAR. 2007. Informe del estado de los ambientes marinos y costeros en Colombia: Año 2006. Serie de publicaciones periódicas Nº 8. Santa Marta, 378 p.
11. Alzate, A., Llanes, T. J., Rodríguez-Moreno, M., Zapata, F.A. 2006. Contri-buciones al Conocimiento del Estado, Funcionamiento y Dinámica de las Comunidades de Peces en Formaciones Coralinas del Pacifico Colombiano: 127-134. In: INVEMAR. 2006. Informe del estado de los ambientes marinos y costeros en Colombia: Año 2005. Serie de publicaciones periódicas No 8. Santa Marta, 360p.
AUTHOR AFFILIATION AND CONTACT INFORMATION
Adriana Alzate Vallejo
Theoretical Research in Evolutionary Life Sciences, Groningen Institute for Evolutionary Life Sciences, University of Groningen, Nijenborgh 7, 9747 AG, Groningen, The Netherlands. Terrestrial Ecology Unit, Department of Biology, Ghent University, K. L. Ledeganckstraat 35, B-9000 Ghent, Belgium.
e-mail: adria.alzate@gmail.com
Karen Bisschop
Theoretical Research in Evolutionary Life Sciences, Groningen Institute for Evolutionary Life
Sciences, University of Groningen, Nijenborgh 7, 9747 AG, Groningen, The Netherlands.
Terrestrial Ecology Unit, Department of Biology, Ghent University, K. L. Ledeganckstraat
35, B-9000 Ghent, Belgium. e-mail: karen.bisschop@ugent.be
Dries Bonte
Terrestrial Ecology Unit, Department of Biology, Ghent University,
K. L. Ledeganckstraat 35, B-9000 Ghent, Belgium. e-mail: dries.bonte@ugent.be
Rampal Etienne
Theoretical Research in Evolutionary Life Sciences, Groningen Institute for Evolutionary Life Sciences, University of Groningen, Nijenborgh 7, 9747 AG, Groningen, The Netherlands. e-mail: r.s.etienne@rug.nl
Thijs Janzen
Institut für Biologie und Umweltwissenschaften. Carl von Ossietzky Universität Oldenburg, Carl von Ossietzky-Str. 9-11, 26111 Oldenburg, Germany.
e-mail: thijsjanzen@gmail.com
James Rosindell
Department of Life Sciences, Imperial College London, Silwood Park Campus, Buckhurst Road, Ascot SL5 7PY, UK.
Fons van der Plas
Institut für Spezielle Botanik und Funktionelle Biodiversität, Universität Leipzig, Johannis-allee 21,
04103 Leipzig, Germany.
e-mail: fonsvanderplas@gmail.com
Fernando A. Zapata
Coral Reef Ecology Research Group, Departamento de Biología, Universidad del Valle, Apartado Aéreo 25360, Cali, Colombia.
