The Population Consequences of Sex and Conflict

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The Population Consequences of Sex and &RQÀLFW

Daniel 5DQNLQ

Helsinki2007

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The Population Consequences of Sex and &RQÀLFW

Daniel 5DQNLQ

Academic Dissertation

To be presented, with the permission of the Faculty of Biociences of the University of Helsinki, for public examination in lecture room 1041 in

Biokeskus 2, Viikinkaari 5, Helsinki, on 26 January 2007 at 12 noon.

Helsinki2007

Laboratory of Ecological and Evolutionary Dynamics Department of Biological and Environmental Sciences

University of Helsinki Finland

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ISBN 952-92-1422-7 (paperback) ISBN 952-10-3594-3 (PDF)

Layout: Daniel J. Rankin Cover Image: Diana Cousminer

Helsinki University Printing House Helsinki 2007

Author’s address:

Laboratory of Ecological and Evolutionary Dynamics Department of Biological and Environmental Sciences P.O. Box 65 (Viikinkaari 1)

FI-00014 University of Helsinki Finland

Homepage: www.rankin.sk (PDLOGDQLHOUDQNLQ#KHOVLQNL¿

daniel@rankin.sk

7KH3RSXODWLRQ&RQVHTXHQFHVRI6H[DQG&RQÀLFW Daniel J. Rankin

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The thesis is based on thefollowing articles, which are referred in the text by the respective chapter numbers:

1. Rankin, D.J. & López-Sepulcre, A. (2005) Can adaptation lead to extinction?Oikos111: 616-619

2. Rankin, D.J. (2007) Resolving the tragedy of the commons: the feedback EHWZHHQ LQWUDVSHFL¿F FRQÀLFW DQG SRSXODWLRQ GHQVLW\Journal of Evolutionary Biology.20: 173-180

3. Rankin, D.J., López-Sepulcre, A., Foster, K.R. & Kokko, H. (2007) Spe- FLHVOHYHOVHOHFWLRQUHGXFHVLQWUDVSHFL¿FFRQÀLFW6XEPLWWHG*

4. Rankin, D.J. & Kokko, H. (2006) Sex, death and tragedy. Trends in Ecol- ogy and Evolution 21: 225-226

5. Rankin, D.J. & Kokko, H. (2007) Do males matter? The role of males in population dynamics. Oikos. (In Press)

6. Rankin, D.J. & Arnqvist, G. (2007) Sexual dimorphism is associated with SRSXODWLRQ¿WQHVVLQWKHVHHGEHHWOHCallosobruchus maculatus. (Submitted) 7. Kokko, K. & Rankin, D.J. (2006) Lonely hearts or sex in the city? Den- sity-dependent effects in mating systems. Philosophical Transactions of the Royal Society of London: Biological Sciences361: 319-334.

*Note:Chapter 3 has been retitled from the above, and is currently submitted as “Species-level selection UHGXFHVVHO¿VKQHVVWKURXJKFRPSHWLWLYHH[FOXVLRQ´

The Population Consequences of Sex and &RQÀLFW

Daniel 5DQNLQ

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&RQWULEXWLRQV

Key:DR: Daniel J. Rankin, HK: Hanna Kokko, AL: Andrés López-Sepulcre, KF: Kevin R. Foster, GA: Göran Arnqvist

Supervised by

Professor Hanna Kokko

University of Helsinki

Finland Reviewed by

Professor Stuart West

University of Edinburgh

United Kingdom

Professor Per Lundberg

University of Lund

Sweden Examined by

Dr Tom Tregenza

University of Exeter

United Kingdom

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Lay Summary Acknowledgements Summary

1. Can adaptation lead to extinction?

2. Resolving the tragedy of the commons: the feedback be- WZHHQLQWUDVSHFL¿FFRQÀLFWDQGSRSXODWLRQGHQVLW\

3.6SHFLHVOHYHOVHOHFWLRQUHGXFHVVHO¿VKQHVVWKURXJKFRP- petitive exclusion*

4. Sex, death and tragedy

5. Do males matter? The role of males in population dynam- ics

6. 6H[XDOGLPRUSKLVPLVDVVRFLDWHGZLWKSRSXODWLRQ¿WQHVV in the seed beetle Callosobruchus maculatus

7. Lonely hearts or sex in the city? Density-dependent effects in mating systems

*Note:Originally titled “6SHFLHVOHYHOVHOHFWLRQUHGXFHVLQWUDVSHFL¿FFRQÀLFW´.

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3UH=RMLþNX

-GLDRWHYĜLGYHĜH

I kdydby tam byla jen Tíkající tma, i kdydby tam bylo jen duté vanutí

i kdyby tam nic nebylo,

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Mirsoslav Holub (1962)

*RDQGRSHQWKHGRRU Even if there’s only the darkness ticking, even if there’s only the hollow wind, even if

nothing is there,

JRDQGRSHQWKHGRRU At least

there’ll be DGUDXJKW

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Lay Summary

The Population Consequences of

Sex and &RQÀLFW

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In the years both during and leading up to my PhD I have been blessed to have crossed paths with many amazing people who have inspired, encourage and stood by me.

7KH¿UVWZKRGHVHUYHPHQWLRQKHUHLV+DQQD for all the effort she has put in to these projects and who through all of the ups and downs of this thesis put in her best to motivate and stimulate me, create a stimulating and exciting environment in which to work.

Andrès remained a good friend, who came to my rescue a number of times. I want to thank him for the friendship, and being a good collaborator, and even if we both had strong views on our ideas, we always worked them out in the end! Also in WKHJURXS.DWMD+,UMD-RQDWKDQ/DXUHQWDQG Tovè were all there for stimulating chats, and of-

¿FHDQWLFV7KDQNVWR-RVWHLQIRUWKHPDQ\EHHUV discussions and strange ideas. Thanks to Kevin for the collaboration and I am still sorry those Finns made us give the bust of that president back, despite it being planned brilliantly.

Thanks to Göran, for the collaboration and the opportunity to come to Uppsala and work in KLVJURXS7KDQNVDOVRWR'DPLDQ-RKDQQD$OH[

and Urban for making my time there interesting.

ĆDNXMHP,YHD5DGNH]DWRåHVDSRVWDUDOLDE\

QHEROD8SSVDODFH]GOKpDWPDYp]LPQpYHþHU\

iba o chrobákoch.

I would also like to thank Veijo, for sorting out the important things, putting up with my relentless enquires about the administration, and being one of the biggest supporters of our, now dissembled, post-seminar drinks. I am grateful to 6WX:HVWDQG3HU/XQGEHUJIRUDJUHHLQJWREHP\

pre-examiners, and to Tom Tregenza for agreeing to be my opponent.

Katja was always there when I needed, and has been a good friend since the moment I arrived.

She helped a lot in all of the thesis work, whether it was listening to my rants about science, giving comments on manuscripts or recommending LQWHUHVWLQJ¿OPVRUQRYHOV

1RQH RI WKLV ZRXOG KDYH EHHQ ¿QLVKHG RQ time if it wasn’t for the amazing encouragement, humour and friendship of Mandy, both before and throughout the writing up. Thanks to Diana for all the cwaffee, the support and the image on the cover. I would also like to thank all of the other members of Thespians Anonymous for the last two years of friendship, the great times we shared, and of course the plays! I can safely say that without their company I may well have gone mad! Similar thanks goes to the members of WKH+HOVLQNL'HEDWLQJ6RFLHW\DQGLQSDUWLFXODU Søren, Scott and Gabe. Thanks to Tiina for all her encouragement and the many cups of tea.

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VSRORþQRVĢ D EOi]QLYp FKYtOH VWUiYHQp Y RNROt Kallio.

I would like to thank the many people in, and associated with, the department in Viiki that I have become friends with over the years, particularly Mike (who also was there to discuss large parts RIWKHZRUN1RH-RKDQ%RE2¶+%RE:DQG /DXUD3DXODZDVDOZD\VWKHUHDVDIULHQGWRJR for coffee or a drink with (even though I was probably always late!), and I want to thank her IRUWKRVHWLPHV%LJWKDQNVWR$FHIRUDOOWKRVH amusing nights, his friendship and always being up for fun.

I would like to thank my friends abroad, who have been there in the background on trips to 6ORYDNLDRUWKH8.$OH['DYH:'DYH0F0 (VWKHU-XOLDQD/DDYDQ\DQ5RELDQG6WXIRUDOO the sporadic, but inspiring, meetings and crazy conversations, usually with plenty of beer, wine, FRIIHHRUDOORIWKHDERYH5RELSDUWLFXODUO\LQ-

Acknowledgments

“

I shambled after as I’ve been doing all my life after people who interest me, because the only people for me are the mad ones, the ones who are mad to live, mad to talk, mad to be saved, desirous of everything at the same time, the ones who never yawn or say a commonplace thing, but burn, burn, burn, like fabulous yellow roman candles exploding like spiders across the stars and in the middle you see the blue centerlight pop and everybody goes ‘Awww!’”

-DFN.HURXDFOn the Road 1957)

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spired me in science over the years. Thanks also WR DOO WKH 'XEQLþDQN\ 7KDQNV WR 6RQLD ZKR ZKLOH,ZDV¿QLVKLQJLQ<RUNERWKEHOLHYHGLQPH and encouraged me to try in science. I’d like to WKDQN5LFKDQG-RQIRUWKHPXVLFIULHQGVKLSDQG drinking games over the years, which has lasted despite me living in several different countries for the past 5 years. Also thanks to Simone, who, maybe through a love of Salmiakki, was always just an e-mail/sms away.

-RKQ 5H\QROGV P\ ZRXOGEHVXSHUYLVRU deserves a mention, not least for indulging in a drunken discussion at the beginning of about JURXSVHOHFWLRQZLWK+DQQDDQGPH,ZRXOGDOVR OLNHWRDFNQRZOHGJH5LFKDUG/DZZKRZKLOHLQ

<RUNWDXJKWPHWKH¿UVWDVSHFWVRIWKHRU\DQG encouraged me to develop them, something which led me this far.

Emilia deserves very special thanks, for painting the dark autumn months with summer colours and making the world feel even more exciting and spectacular since we stumbled into each other’s lives.

2IFRXUVH,FRXOGQRWIRUJHWHYHU\WKLQJP\

family has done for me to get me where I am.

9HĐPLUiGE\VRPSRćDNRYDOVYRMPXGHGNRYL ktorý ma obdaroval láskou k vzdelávaniu sa a OiVNRXNKRUiP%DENH]DOiVNXNOLWHUDW~UHNWRU~

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7KH6HO¿VK*HQH

0\SDUHQWV-LPDQG-DUNDKDYHDOZD\VLQ- stilled in me a belief that one can strive for anything, regardless of background, gender or social class. Without their support and encouragement, nothing I have done would have been possible.

)LQDOO\WKDQNVWRP\VLVWHU=RsIRUWKHFKLOG- hood we shared, and to whom I’ve dedicated this thesis.

$OORIWKHZRUNZDV¿QDQFHGE\WKH$FDGHP\

RI)LQODQG*UDQWWR+DQQD.RNNR

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1

Introduction

Natural selection generally operates at the level of WKHLQGLYLGXDORUPRUHVSHFL¿FDOO\DWWKHOHYHORI the gene (Dawkins 1976). As a result, individual selection does not always favour traits which EHQH¿WWKHSRSXODWLRQRUVSHFLHVDVDZKROH7KH spread of an individual gene may even act to the GHWULPHQWRIWKHRUJDQLVPLQZKLFKLW¿QGVLWVHOI HJ3DUWULGJH +XUVW7KXVVHOHFWLRQDW the level of the individual can affect processes at the level of the organism, group or even at the level of the species.

As most behaviours ultimately affect births, deaths and the distribution of individuals, it seems inevitable that behavioural decisions will have an impact on population dynamics and population densities (Sutherland 1996). Behavioural decisions can often involve costs through allocation of energy into behavioural strategies, such as the LQYHVWPHQWLQWRDUPDPHQWVLQYROYHGLQ¿JKWLQJ over resources (e.g. Emlen 2001) or increased mortality due to injury or increased predation risk (e.g. Jakobsson et al. 1995; e.g. Dunn et al.

6LPLODUO\ EHKDYLRXU PD\ DFW WR EHQH¿W the population, in terms of higher survival and increased fecundity. Examples include increased investment through parental care, choosing a mate based on the nuptial gifts they may supply (Arn- qvist & Nilsson 2000; Møller & Jennions 2001) and choosing territories in the face of competition (López-Sepulcre & Kokko 2005).

Investigating the impact of behaviour on population ecology may seem like a trivial task, but it is likely to have important consequences at different levels. For example, antagonistic behaviour may occasionally become so extreme that it increases the risk of extinction (chapter 1 and 4), and such extinction risk may have important implications for conservation (Bennett & Owens 1997; Bessa-Gomes et al. 2003; Fisher & Owens

2004). As a corollary any such behaviour may also act as a macroevolutionary force, weeding out SRSXODWLRQV ZLWK WUDLWV ZKLFK ZKLOVW EHQH¿FLDO to the individuals in the short term, ultimately result in population extinction (chapter 3). In this introduction, I will examine how behaviours, spe- FL¿FDOO\FRQÀLFWDQGFRPSHWLWLRQRYHUDUHVRXUFH and aspects of behaviour involved in sexual selection, can affect population densities, and what the implications are for the evolution and ecology of the populations in question.

The tragedy of the commons

$GDP6PLWKSURSDJDWHGWKHYLHZWKDWWKHVHO¿VK interests of individuals could create harmony, DQGEHQH¿WVRFLHW\DVDZKROH6PLWK+H SRVWXODWHGWKHLGHDWKDWVHO¿VKEHKDYLRXUFRXOG lead to an “invisible hand” which would promote the public interest (Smith 1776). Economists have VLQFHUHDOL]HGWKDWWKLVLVQRWDOZD\VWKHFDVH7KH strongest evidence comes from the over-exploita- tion of common resources, a phenomenon which has come to be known as “the tragedy of the commons” (Hardin 1968). In the tragedy of the commons, disaster arises when herders’ animals graze on common land. If the herders are driven only by self-interest, they will realize that it will be to their advantage to put another animal on the common, as the negative effects of overgrazing ZLOOEHVKDUHGE\DOOODQGXVHUV7KXVLWZLOOEH to the advantage of each herder to add another animal, and eventually a “tragedy” will arise through overgrazing. Hence, Adam Smith’s view WKDWVHOILQWHUHVWZLOOEHQH¿WWKHFRPPXQLW\DVD whole does not apply to individuals exploiting a common resource, and the tragedy of the commons serves as a powerful argument for private ownership, or alternatively, state regulation.

In evolutionary biology, the tragedy of the commons provides a powerful analogy (Dionisio

Summary

Daniel J. Rankin

Laboratory of Ecological and Evolutionary Dynamics, Department of Biological and Environmental Sciences, PO Box 65, FI - 00014, University of Helsinki, Finland

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2

& Gordo 2006). It can be used both to understand WKHFRQVHTXHQFHVRIFRQÀLFWIRUWKHPHPEHUVRI groups and populations, and as a counter point to ask the question of why the tragedy of the commons may not always occur. Hardin (1968) originally used the tragedy of the commons to ar- gue for restrained reproduction in humans. Whilst citing Lack’s work on population regulation (Lack 1954), he remained in the realm of the problems faced by human population growth, and did not venture to extend his analogy to the problems of evolutionary ecology. However, the problem RIZK\LQGLYLGXDOVGRQRWVHO¿VKO\RYHUH[SORLW the resources available to them has remained a problem since the group selection debate (Wil- liams 1966).

Potential evolutionary “tragedies” have been observed in many systems (Gersani et al. 2001;

Falster & Westoby 2003; Wenseleers & Ratnieks 2004; Dionisio & Gordo 2006; Kerr et al. 2006).

Perhaps the most common way of applying Har- din’s ideas to evolutionary biology is in terms of public good contests; if individuals must invest in a public good, a tragedy of the commons will occur if individuals abstain from such invest- PHQWEHQH¿WLQJIURPWKHDFWLRQVRIRWKHUJURXS members. In such a situation, the common good is diminished, and a tragedy of the commons arises. For example, in species which use sentinels to guard and warn other members of the group against predators, it may often be more advantageous to abstain from vigilance so that once may invest more in foraging (Bednekoff 1997; Clut- ton-Brock et al. 1999). In such a case, the tragedy arises if it becomes more advantageous for all members of the group to forage, rather than to protect the group against predators. Similarly, in microbes such as yeast Saccharomyces cerevisiae, common enzymes are often produced which ben- H¿WDOOPHPEHUVRIWKHJURXS*UHLJ 7UDYLVDQR 2004). Yeast produce the enzyme invertase, which is needed for the digestion of sucrose (Greig &

7UDYLVDQR 6HO¿VK VWUDWHJLHV WKDW GR QRW SURGXFHWKLVHQ]\PHJDLQWKHEHQH¿WIURPRWKHU individuals investing in a common good, whilst QRW LQYHVWLQJ WKHPVHOYHV *UHLJ 7UDYLVDQR 2004). Aside from public goods games, there are a number of other ways in which the tragedy of the commons analogy has been applied to evolutionary problems, for example in terms of the

evolution of virulence in host-pathogen interactions (Kerr et al. 2006).

6H[XDOFRQÀLFW

6H[XDO FRQÀLFW RYHU SDUHQWDO FDUH PD\ DOVR EH prone to the tragedy of the commons, where one RUPRUHSDUHQWGHFLGHVLWLVWRWKHLURZQVHO¿VK advantage to abandon their offspring than to share WKHFRVWRIFDULQJIRUWKHP7ULYHUV:KLOH each parent has a shared interest in the welfare of their offspring, it is to the advantage of both the mother and the father to try to delegate care to the other partner (Maynard Smith 1977). It is often the female who invests the most in caring for KHURIIVSULQJ4XHOOHU7KHH[WUDEHQH¿WV gained from having broods with multiple males may favour increased female cuckoldry of her partner (Kokko 1999). In a situation where both parents may/can care for offspring, it would be to the advantage of her partner to care less for the offspring, and rather seek extra matings elsewhere (Kokko 1999).

More recently, the tragedy of the commons has been suggested to arise through male sexual harassment of females (chapter 4). It is known that males can potentially have a very negative LPSDFWRQIHPDOH¿WQHVV)RUH[DPSOHIUHTXHQW mating in Drosophila melanogaster has been shown to reduce female lifespan and reproductive VXFFHVV)RZOHU 3DUWULGJH7KHVHFRVWV have been shown to be caused by a single peptide (Chapman et al. 1995; Wigby & Chapman 2005), which both stimulates female egg production and decreases female receptivity (Chapman et al. 2003; Liu & Kubli 2003). In feral sheep Ovis aries, higher female mortality is associated with male rutting activity, suggesting that male harassment increases female mortality (Réale et al.

1996). It is ultimately polyandry and the resulting male-male competition which results in females suffering from increased male harassment. If we view females as a resource over which males are FRPSHWLQJWKHQZHPD\DOVRYLHZVH[XDOFRQÀLFW as a form of the tragedy of the commons (chapter 4). In male harassment, it is generally the females that pay a cost (in terms of increased mortality), ZKLOHWKHPDOHVEHQH¿WIURPLQYHVWLQJPRUHLQ harassment (by obtaining more fertilizations relative to other males in the population). Under some circumstances one may envisage that it will

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3 always be advantageous for males to invest more

in harassment, a situation which could increase female mortality to the point where the population may no longer persist (Kokko & Brooks 2003).

Such a tragedy of the commons has been al- luded to in the common lizard Lacerta vivipara (Le Galliard et al. 2005). In this study, male and female biased populations were compared, and it was found that there was disproportionately higher female mortality in male-biased, relative to female-biased populations (Le Galliard et al.

7KLVZDVGXHWRPDOHKDUDVVPHQWZKLFK had previously been shown to affect female mortality through biting and stress (Bauwens

& Verheyen 1985; Moore & Jessop 2003). It was predicted that, if the harassment exhibited in male-biased populations were to continue, it would lead to a positive feedback (Crespi 2004), further biasing the sex ratio to the point where the population would be driven extinct (Le Galliard et al. 2005). In chapter 4 of this thesis, I suggest WKDWVH[XDOFRQÀLFWPD\UHVXOWLQDWUDJHG\RIWKH commons, and use the Le Galliard et al. (2005) study to make my case.

&RQÀLFWVLQJHQHUDO

7KH³SULVRQHU¶VGLOHPPD´KDVORQJEHHQXVHGLQ evolutionary biology as a model of cooperation (Maynard Smith 1982). In the prisoner’s dilemma game, two players can choose to either cooperate with each other on a task or “defect” from cooperation. If one individual defects, while the other cooperates, the defector will get a higher payoff than if they both cooperated, but the combined sum of their payoffs would be larger if they both FKRVHWRFRRSHUDWH)URPDVHO¿VKSRLQWRIYLHZ the best option is to defect. We can view defec- tion in the prisoner’s dilemma game as a very ORRVHIRUPRIWKHWUDJHG\RIWKHFRPPRQV7KH tragedy occurs because individuals have a lower productivity under competition than they would LQWKHDEVHQFHRIFRPSHWLWLRQDQGFRQÀLFW:HVW et al. GH¿QHWKHWUDJHG\RIWKHFRPPRQV as “a situation when individuals would do better to cooperate, but cooperation is unstable because HDFKLQGLYLGXDOJDLQVE\VHO¿VKO\SXUVXLQJWKHLU own short-term interests”, which is the essence of WKHSULVRQHU¶VGLOHPPD7KHVDPHSULQFLSOHFDQ be true of other games, such as the hawk-dove game (Maynard Smith 1982).

Competition with other individuals over a resource may lead to a situation where investment in traits to compete for the resource will incur a fecundity or survival cost. One classical example comes from plant competition (Haldane 1932), where taller plants have more access to light (Haldane 1932; Falster & Westoby 2003;

Dieckmann & Ferrière 2004). As a result of competition for light, any individual which can grow larger than its counterparts will have a selective advantage (Falster & Westoby 2003). However, it may be that investing in growth takes resources away from reproduction, and so a situation may arise where fecundity is reduced to such an extent that the population becomes unviable – the individual level competition for light has given rise to a tragedy of the commons. Such a scenario can be seen as a tragedy of the commons because competition among the individual plants results in a situation were it is better for each plant to have a much lower fecundity than in the absence of competition. While there is no common that is destroyed, it is the fact that the group fares worse under competition that makes this a tragedy of the commons: had they all agreed to “cooperate” and back down, they would each be able to invest more in fecundity, rather than investing in competition.

Another example of the tragedy of the com- PRQVDVDUHVXOWRIFRQÀLFWFRPHVIURPPLFURELDO warfare. Some bacteria produce bacteriocins, which are proteins with a range of antimicrobial killing activity that is often limited to conspecif- LFV5LOH\ :HUW]5LOH\HWDO7KH production of such agents inevitably bears a cost, which may come in the form of diverting resources from other cellular functions or ultimately in the death of the producing individual 5LOH\ :HUW]7KHXVHRIVXFKFKHPLFDO weapons can be seen as a tragedy of the commons, as the population as a whole is worse off due to bacteriocin meditated death, in addition to bearing the costs of bacteriocin production. All members of the population could collectively do better to

“cooperate” and not invest in bacteriocins, rather than communally pay the costs of investing in competition.

In situations involving competition with con- VSHFL¿FVVWUDWHJLHVZKLFKGRZHOOUHODWLYHWRRWKHU members of the population, but result in a reduc-

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4

tion in absolute fecundity and survival, will be IDYRXUHGFKDSWHU FKDSWHU7KXVDQ\IRUP RIFRPSHWLWLRQDQGFRQÀLFWPD\EHVHHQWROHDG to a tragedy of the commons, particularly when WKHOHYHORIFRQÀLFWSRVHVDWKUHDWWRSRSXODWLRQ persistence (chapter 1).

Evolutionary suicide

,IFRQÀLFWZLWKLQDSRSXODWLRQFDQHYROYHWREH VR H[WUHPH WKDW LW H[HUWV D ODUJH LQÀXHQFH RQ absolute fecundity and survival, there is the possibility that it may drive the population extinct (chapter 1). Such extinction has come to be labeled “evolutionary suicide” (Ferrière 2000;

Gyllenberg & Parvinen 2001; Gyllenberg et al.

2002; Dieckmann & Ferrière 2004; Parvinen 2005). Evolutionary suicide may occur in three potentially different ways, but the outcome, namely population extinction, remains the same in all three. As evolutionary suicide remains to be tested in a controlled way (chapter 1), for the ben- H¿WRIHPSLULFLVWVLWZRXOGKHOSWRJURXSDOOWKUHH scenarios under the same term (see chapter 1 for details). Individual level selection can also lead to a gradual decline in population densities (such as in the model presented in chapter 2), where the population is taken to a level where it can no ORQJHU VXVWDLQ LWVHOI7KLV PD\ KDSSHQ WKURXJK Allee effects (Dennis 2002) or demographic or environmental stochasticity (Saether & Engen 2004). However, in a purely deterministic system, the only way in which evolution can cause extinction is through a sudden and abrupt extinction (Gyllenberg & Parvinen 2001). In other words, as different traits spread through the population, WKH\LQÀXHQFHWKHHTXLOLEULXPSRSXODWLRQGHQVLW\

As evolution converges to a point, the population may cross a threshold where an equilibrium population density is not possible, such as extreme levels of female mortality caused by male harassment (D. Rankin unpublished data - see also chapter 5), and the population crashes.

(YLGHQFHIRUHYROXWLRQDU\VXLFLGH

Chapter 1 of this thesis describes some studies which allude to evolutionary suicide. Owing to WKHGLI¿FXOW\RIGHWHUPLQLQJWKHH[DFWFDXVHRI any extinctions we might observe in nature or

the laboratory, there is very limited empirical evidence for evolutionary suicide, and what evidence there is remains somewhat circumstantial (chapter 1). In chapter 1 of this thesis, I make the case that evolutionary suicide should be taken seriously as an evolutionary force, and propose some examples which seem to support the idea.

Comparative studies may help us understand which traits may have an impact on population processes. For example, a comparative study in birds found that testes size, a useful indicator of the intensity of sperm competition, was correlated with extinction risk in birds (Morrow & Pitcher 2003). Another comparative study, this time cor- relating the size of plant genomes with extinction risk showed that the there was a positive correlation between genome size and the risk of extinction (Vinogradov 2003; Vinogradov 2004b). As a larger genome size is thought to be indicative RIWKHDPRXQWRIVHO¿VK'1$9LQRJUDGRY Vinogradov 2004b; Vinogradov 2004a), this would seem to support the notion that gene-level selection may result in a situation which puts the population at a greater risk of extinction. In the social bacterium Myxocococcus xanthus individuals cooperate to form complex fruiting structures where the spores from the fruiting body disperse to form new colonies (Fiegna & Velicer 2003).

$UWL¿FLDOO\VHOHFWHGFKHDWHUVWUDLQVZKLFKZHUH more likely to become spores, were shown to have an advantage over wild-type strains. It has been shown that, under certain conditions, these strains could invade a wild-type population and drive the entire population extinct (Fiegna & Velicer 2003).

7KHODFNRIFOHDUVWXGLHVGHPRQVWUDWHVWKDWH[SHUL- ments are still required to test for the impact of individual-level selection on extinction risk.

:K\GRHVSRSXODWLRQGHQVLW\PDWWHU"

Understanding how behaviour affects processes at the level of the population allows us to investigate the consequences of individual behaviour for a wide range of processes, such as conservation or macroevolution (see below). From a conservation point of view, small populations are more vulner- able to extinction than large populations (Soulé 1987). Small populations may be driven extinct by Allee effects and the risks posed by demographic and environmental stochasticity (Stephens &

Sutherland 1999; Dennis 2002; Drake & Lodge

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5 2004; Saether & Engen 2004). Small populations

are also more prone to inbreeding (Saccheri et al.

1998; Keller & Waller 2002) or mutational melt- down, as deleterious mutations are more likely WR¿[DWHDWORZHUSRSXODWLRQGHQVLWLHV/\QFK

*DEULHO7KXVDQ\IDFWRUZKLFKUHGXFHVWKH population size also brings a population closer to the extinction threshold.

7KHEHKDYLRXURILQGLYLGXDOVFDQDOVRDIIHFW other population processes. For example, adaptive processes may also have an effect on cycling and oscillatory population dynamics (Greenman et al. 2005). In addition to affecting the type of population dynamics, adaptive behaviour can DOVRLQÀXHQFHWKHVWDELOLW\RISRSXODWLRQG\QDP- ics (McNamara 2001). As unstable or cycling population dynamics are more likely to go extinct, we must not only pay attention to the number of individuals in a species or population, but also to the nature of the population dynamics themselves.

However, for simplicity I only investigate the effect of behaviour the on overall population density in this thesis.

The role of sex in population dynamics

2QHVSHFL¿FZD\LQZKLFKLQGLYLGXDOOHYHOEH- haviour may affect population density is where sexual reproduction is involved. Explaining how sexual reproduction may have arisen by natural selection is one of the biggest challenges in evo- OXWLRQDU\ HFRORJ\ 0D\QDUG 6PLWK 7KH reason for this is that a gene propagating itself via asexual reproduction will have a two-fold advantage (Maynard Smith 1978) over a gene that propagates itself via sexual reproduction.

7KDWDOUHDG\FRQVWLWXWHVDSRZHUIXOFRVWWRDJHQH ZKLFKUHSURGXFHVVH[XDOO\7KHVDPHLVWUXHIRU individuals involved in the messy business of sexual reproduction. Given all of the complica- WLRQVRIVH[VXFKDV¿QGLQJDPDWHRIWKHRSSRVLWH sex, attracting that mate, competing for a mate, sharing the care over offspring and dealing with your mate trying to eat (Prenter et al. 2006), hurt (Crudgington & Siva-Jothy 2000) or cuckold (Komdeur 2001) you, one can see that sexual UHSURGXFWLRQFDQEHDYHU\FRVWO\EXVLQHVV7KLV is true whether we think at the level of individual genes, or at the level of the species itself, and

VH[XDOEHKDYLRXUFDQHYHQKDYHDQLQÀXHQFHRQ extinction risk (Kokko & Brooks 2003).

6H[DQGSRSXODWLRQG\QDPLFV

In models of population dynamics, one typically assumes that males do not “matter” to births and deaths (chapter 5). In other words, it is assumed that the presence/absence of males does not affect female birth rates, and they contribute to death to the same extent as females, allowing us to scale population density by one half. However, given the potential costs of sex, one should expect males WRPDWWHULQDWOHDVWVRPHVLWXDWLRQV7KHPRVWED- sic of these is that if females are always fertilized, and males and females consume the same amount of resources, removing males from the population will leave more “space” for females, and hence population density will increase. Chapter UHYLHZVKRZWKHSUHVHQFHRIPDOHVLQÀXHQFH population densities.

0DOHKDUDVVPHQWPD\DOVRKDYHDQLQÀXHQFH on the number of females in a population (chapter 4), and this will change with the proportion of males and females in the population. However, the presence or absence of males can also affect population densities in other ways (chapter 5). For H[DPSOHLQWHQVLYHVH[VSHFL¿FKXQWLQJRIPDOH Saiga Antelope Saiga tatarica for their horns can result in a situation where there are so few males LQWKHSRSXODWLRQWKDWIHPDOHVDUHXQDEOHWR¿QG a mate (Milner-Gulland et al. 2003). In contrast to this, populations of the Independent Samoan EXWWHUÀ\Hypolimnas bolina are able to persist despite the widespread presence of male-killing Wollbachia, which led to extreme sex ratios al- most devoid of males (Dyson & Hurst 2004).

7KHSUHVHQFHRUDEVHQFHRIPDOHVFDQLPSDFW the intensity of density dependence, as males from populations where males are larger than females will require more resources than females (chapter 5). In ungulates in particular, the differences in resource use between males and females can be so strong that they also pose interesting management questions, such as how much of each sex one should harvest to keep the population sustainable (Mysterud 2000; Clutton-Brock et al. 2002). Other forms of sexual dimorphism are DOVRSUHGLFWHGWRKDYHDQLQÀXHQFHRQSRSXODWLRQ densities (chapter 5, chapter 6). Due to the costs involved in sexual selection, one should expect

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6

increased sexual dimorphism to be negatively associated with population densities (Morrow

& Pitcher 2003; Kokko and Brooks 2003; Mor- URZ )ULFNH7KHVHFRVWVFDQEHLQGLUHFW where attractive males yield less viable offspring (Brooks 2000), or direct, such through male harm (Chapman et al. 1995; Crudgington & Siva-Jothy 2000).

,QFRQWUDVWIHPDOH¿WQHVVPD\EHLPSURYHG E\GLUHFWEHQH¿WVVXFKDVZKHUHPDOHVSURYLGHG nuptial gifts of care for offspring, (Møller &

Jennions 2001; Arnqvist et al. 2005), or indirect JHQHWLFEHQH¿WVRIIHPDOHVPDWLQJPXOWLSO\.R- QLRUHWDO7UHJHQ]D :HGHOORUZLWK males with good genes (Promislow et al. 1998;

Head et al. 2005). Any trait which improves fe- PDOH¿WQHVVVKRXOGXOWLPDWHO\LQFUHDVHSRSXODWLRQ

¿WQHVVFKDSWHUPHDQLQJWKDWVH[XDOVHOHFWLRQ may actually have a positive, rather than negative, effect on population densities.

,QWUDORFXVVH[XDOFRQÀLFW

,QWUDORFXV VH[XDO FRQÀLFW ZKHUH DQ DOOHOH DW D single locus codes for different phenotypes in males and females, can also affect population GHQVLWLHVFKDSWHU7KLVFDQRFFXULIWKHH[SUHV- sion of an allele expressed in both sexes is in a state of “compromise” (Chippindale et al. 2001).

In other words, males and females carrying the WUDLWVDUHQRWDWWKHLUSRWHQWLDO¿WQHVVRSWLPD$

VWURQJHUXQUHVROYHGFRQÀLFWZRXOGEHLQGLFDWHG if the respective male and female phenotypes were less dimorphic and constrained to be similar. Less dimorphism, where males and females are less FRQVWUDLQHGDQGWKHUHIRUHDWWKHLUUHVSHFWLYH¿W- ness optima, would be an indication that the con- ÀLFWZDVZHDNHURUDEVHQW5LFH &KLSSLQGDOH ,QWUDORFXVVH[XDOFRQÀLFWFDQEHUHVROYHG through adaptation by the rest of the genome and evolutionary changes in genetic architecture (Bonduriansky & Rowe 2005). As a resolved FRQÀLFWPHDQVWKDWIHPDOHVDQGPDOHVKDYHERWK UHDFKHGWKHLU¿WQHVVRSWLPDZHZRXOGWKHUHIRUH expect females to produce more offspring, and the population to have a higher density.

Chapter 6 presents a study using 13 populations of the beetle Callasobruchus maculatus, where each population had a different evolutionary history. In this chapter I looked at various indicators of sexual dimorphism (e.g. size, shape

and colour) and investigated the relationship to juvenile (the proportion of eggs developing to DGXOWKRRGDQGDGXOW¿WQHVVWKHWRWDOQXPEHURI adults emerging). As a positive relationship was found, I suggest that this could in fact be explained E\LQWUDORFXVVH[XDOFRQÀLFWEXWLWLVOLNHO\WKDW other mechanisms could be playing a role in the pattern observed. Whatever the explanation, it is FOHDUIURPFKDSWHUVWKDWVH[FDQKDYHDGH¿QLWH LQÀXHQFHRQSRSXODWLRQSURFHVVHV

What may resolve the tragedy?

When we think about the tragedy of the commons and population extinction, we must ask what prevents such phenomena occurring (chapter 1).

As mentioned above, there are a range of situa- WLRQV ZKHUH FRQÀLFW PD\ UHVXOW LQ ORZHU JURXS productivity and increases in the likelihood that a population will be driven extinct. On the other hand, we can observe large amounts of cooperation within and between organisms, which we VKRXOGH[SHFWWREHEURNHQGRZQE\WKHVHO¿VK LQWHUHVWV RI IUHH ULGHUV DQG FKHDWHUV7KHUHIRUH in this thesis I have also addressed processes that could resolve the tragedy (chapters 2 and 7) or OLPLWWKHLQWHQVLW\RIFRQÀLFWVWKDWZHREVHUYHLQ nature (chapters 2 and 3).

:K\LQGLYLGXDOVGRQRWVHO¿VKO\GHVWUR\WKH common good has long been an important question in both sociobiology (Leigh 1977; Frank 1995; Keller 1999) and the social sciences as D ZKROH )LQOD\VRQ 7KLV SUREOHP ZDV proposed long ago in terms of human societies E\7KRPDV+REEHVZKRDUJXHGWKDWLWZDVODZ maintained by the use of force and punishment, that kept social order (Hobbes 1660). However, in human societies, one can frequently observe people keeping to a social norm even when the cost of punishment is very low relative (Finlayson 2005). As a result, it is not just coercion which can act to prevent the tragedy of the commons in human-exploited resources, and individual morality and social norms should also be seen as equally important factors.

7KHUHDOL]DWLRQWKDWDSHUVRQVXWLOLW\ZDVPDGH up of more than just monetary self-interest has long been realized by economists (Becker 1992).

%LRORJLVWVKDYHDPXFKHDVLO\GH¿QHGXWLOLW\WR use when studying the behaviour of their organ-

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7 LVPVQDPHO\¿WQHVV+HQFHLQQDWXUHWKHUHDUH

no morals, and we can see natural selection as proceeding purely by individual self-interest; if LQGLYLGXDOVGRQRWDFWWRPD[LPL]HWKHLU¿WQHVV they will be selected against. Given the “self-interest” of individual genes, the problem of how the tragedy of the commons might be resolved remains even more perplexing.

One of the most invoked mechanisms whereby FRQÀLFWVPD\EHUHVROYHGLVLQWHUPVRINLQVH- lection (Hamilton 1964). If individuals interact locally with other highly related individuals, such as in group structured populations, then lower OHYHOVRIFRQÀLFWZLOOEHIDYRXUHG)UDQN Kin selection is likely to be important in any situation where populations are structured in some way, such as into groups (Wilson 1975) or on a lattice (Nowak & May 1992). Spatial structure is also important and has the effect of increasing the amount of repeated interactions by the same individuals (Nowak & May 1992; Killingback et al. 1999).

As in human societies, coercion, in the form of pressure from other individuals, has been shown to be a potential force in the repression of competition (Frank 1995). Behaviours such as policing have been shown to have evolved in some social insects (Wenseleers et al. 2004;

Ratnieks & Wenseleers 2005), where “policing”

individuals ensure that colony workers act to the EHQH¿WRIWKHZKROHFRORQ\DQGGRQRWUHSURGXFH IRUWKHLURZQVHO¿VKLQWHUHVW

Pleiotropy, where one gene affects multiple traits, is both extremely common in all genomes and highly variable in its effects (Foster et al.

2004). When a pleiotropic relationship ties a SRWHQWLDO VHO¿VK WUDLW WR D SHUVRQDO FRVW LQ WKH JHQRPHWKLVZLOOUHGXFHWKHLQFHQWLYHIRUVHO¿VK- ness. For example, the social amoeba Dictyostel- ium discoideum forms social aggregations where some cells die in an apparent act of altruism to form a stalk that allows other cells to disperse as spores. Pleiotropy of the gene dimA reduces WKHLQFHQWLYHWRVHO¿VKO\IRUPVSRUHUDWKHUWKDQ stalk, cells by linking the altruistic act of stalk production to the ability to make spores (Foster HWDO7KLVOLPLWVWKHHYROXWLRQRIFKHDWHUV that produce fewer stalk cells.

If additional investments in competition bring smaller and smaller rewards, higher levels of con-

ÀLFWZLOOEHGLVDGYDQWDJHRXV)RVWHU6XFK diminishing returns are likely to be common in a range of organisms, particularly when the individuals cannot make full use of the extra resources that they acquire (Foster 2004). For example, self- ishly abstaining from blood sharing by vampire bats is likely to be subject to diminishing returns (Foster 2004). In this case, bats which are full are QRWDEOHWRPDNHHI¿FLHQWXVHRIDOORIWKHEORRG DQGKHQFHWKH\ZLOOEHQH¿WOHVVIURPQRWVKDULQJ with other individuals (Wilkinson 1984).

A similar phenomena to diminishing returns that is also likely to be important in reducing the LQWHQVLW\RIFRQÀLFWVLVZKHQWKHUHLVDIHHGEDFN between the size of the population/group and the LQWHQVLW\ RI FRQÀLFW FKDSWHU ,I FRQÀLFW DQG competition can have a negative impact on the number of individuals in a population, then this will change the number of individuals there are to interact with, ultimately affecting the structure RIWKH³JDPH´FKDSWHUFKDSWHU7KHUHLVQR reason to assume that selective pressures will be the same at low densities as they are at high densities, and there will therefore be a feedback between adaptive individual behaviour and SRSXODWLRQGHQVLW\7KHVWUHQJWKRIWKLVIHHGEDFN FRXOGWKHUHIRUHKDYHDQLQÀXHQFHRQWKHVWUHQJWK RIWKHFRQÀLFWLWVHOIDQGPD\EHDUHDVRQZK\WKH population is not driven extinct (chapter 2).

In chapter 7 I suggest that the number of individuals in a population may be important in sexual VHOHFWLRQDQGVH[XDOFRQÀLFW.RNNRDQG%URRNV SUHVHQWDVLPSOHPRGHORIVH[XDOFRQÀLFW where they assume a trade-off in a trait that gives males a higher competitive ability by enhancing mating success while reducing fecundity when H[SUHVVHGLQDIHPDOH7KHPRGHOVKRZHGWKDW under certain conditions, alleles which resulted in higher male competitive ability could spread, but the resulting cost to females was enough to drive the population extinct. In an extension of WKLVPRGHO,VKRZWKDWLIWKHEHQH¿WPDOHVJDLQ from coercion of females depends on population density, this feedback can be enough to potentially prevent the population from going extinct and may resolve the tragedy of the commons (chapter 7). Extending this notion further, but with a more JHQHUDOFRQÀLFW,VKRZWKDWWKHGHJUHHWRZKLFK WKHEHQH¿WVRILQYHVWLQJLQFRQÀLFWDUHGHQVLW\

dependent can prevent extinction. More interest-

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8

ingly, in cases where extinction would have oc- curred, the strength of this feedback acts to reduce WKHRYHUDOOOHYHORIFRQÀLFWLQFUHDVLQJWKHRYHUDOO VL]HRIWKHSRSXODWLRQFKDSWHU7KHVWUHQJWK of the feedback between population density and WKHLQWHQVLW\RIWKHFRQÀLFWKDVWKHSRWHQWLDOWREH DQLPSRUWDQWEXWRYHUORRNHGFRQÀLFWUHVROYLQJ mechanism (chapter 2).

Macroevolutionary consequences RIFRQÀLFW

&RQÀLFWDQGLQSDUWLFXODUVH[XDOFRQÀLFWKDVEHHQ invoked as a potential mechanism of speciation (Parker & Partridge 1998), for example through reproductive isolation (Martin & Hosken 2003).

+RZHYHU WKH UROH RI FRQÀLFWPHGLDWHG H[WLQF- tion as a potential macroevolutionary force has remained less explored. If individual-level con- ÀLFWFDQKDYHDQHIIHFWRQSRSXODWLRQGHQVLWLHV then there is the possibility that it could act as a macroevolutionary force (chapter 1 and chapter 3). Anything which reduces population densities is likely to bring that population closer to extinction (Soulé 1987), and over long evolutionary timescales will be likely to increase the probability that the species in question will be GULYHQH[WLQFW7KHLGHDWKDWVHOHFWLRQFDQWDNH place at the level of the species is not a new idea (Wynne-Edwards 1962), however it has been argued that such selection should be relatively weak and infrequent to counter individual-level selection (Williams 1966; Maynard Smith 1976).

7KHLGHDWKDWVHOHFWLRQFDQWDNHSODFHDWKLJKHU levels has been largely dismissed (but see Lloyd

& Gould 1993; Gould & Lloyd 1999; but see Nunney 1999), and currently the majority of papers advocating a “group selection” approach apply deme-level selection (Wilson 1975), which has been formally shown to be analogous to kin selection (Queller 1992).

In light of recent work demonstrating evolutionary suicide (chapter 1, Matsuda & Abrams 1994; Gyllenberg & Parvinen 2001; Gyllenberg et al. 2002; chapter 1, Dieckmann & Ferrière 2004), the idea of selection acting at the level of the population or of the species should once more be taken seriously, as evolutionary suicide itself could act as a potential selective pressure among species (chapter 1, chapter 3). Chapter

3 of this thesis presents a model which dem- onstrates that evolutionary suicide can act as a VHOHFWLYHIRUFH RI LWV RZQ$OORZLQJ FRQÀLFW WR evolve in a given species, it is shown that life-history “constraints” or “species properties”, which result in the population evolving higher levels RIFRQÀLFWE\LQGLYLGXDOOHYHOVHOHFWLRQZLOOEH selected against at the species level, as they will be more likely to drive the population extinct. As the Russian Anarchist Peter Kropotkin remarked

“the unsociable species…are doomed to decay”

(Kropotkin 1902).

As mentioned above, selection at the level of the species has been argued to be a weak force when acting in opposition to individual-level selection (Williams 1966). However, this neglects the fact that species do not exist in isolation;

they must also be robust against environmental stochasticity and competition with other species.

Incorporating a very simple form of community assembly into such models of species-level selection increases the extinction risk, thus intensify- ing the strength of species-level selection. As a theoretical expectation, species where individuals XQGHUJRKLJKOHYHOVRIVRFLDOVWULIHDQGFRQÀLFW will not fare well against other competitors (chapter 3).

One could also see species-level selection as D³FRQÀLFWOLPLWLQJ´PHFKDQLVPWKHSRSXODWLRQV ZKLFKHYROYHGWRRKLJKFRQÀLFWVDUHHYHQWXDOO\

driven extinct, meaning that what we observe in nature should be seen as a product of both individual-level and species-level selection (chapter 3). It is the realisation that community dynamics may intensify higher-levels of selection that makes species-level selection more plausible.

Hence, the strength of species-level selection may EHVWURQJHUWKDQSUHYLRXVO\WKRXJKW7KHREYLRXV GLI¿FXOWLHV RI REVHUYLQJ WKH FDXVHV RI D JLYHQ extinction make empirical testing of such theo- ries a challenge. However, this does not exclude species-level selection as an important force in shaping the patterns we observe in nature.

Conclusion

In this thesis, I examine how behaviour at the level of the individual can affect processes DWWKHOHYHORIWKHSRSXODWLRQFKDSWHUV7KH JHQHUDO¿QGLQJRIWKHWKHVLVLVWKDWFRQÀLFWFDQ

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9 have a negative impact on population densities

(chapters 2-3 and 5-6). However, as has been discussed in some of the chapters, behaviour can also have a positive impact on population densities, such as when males provide a direct EHQH¿WWRIHPDOHVFKDSWHUVDQG7KHVWXGLHV in this thesis have only scratched the surface of what is yet to be discovered. I have used a simple proxy, population density, as an indicator of how behaviour affects population processes. In this thesis I did not explore time-to-extinction in the various models, and did not investigate how other factors of population density, such as stability (McNamara 2001), are likely to be affected by individual behaviour.

2QH LPSRUWDQW ¿QGLQJ LV WKDW DQ\ VWUDWHJ\

which has an effect on population processes is, by altering the extinction risk of its own population, likely to subject itself to higher levels of selection (chapter 3). In the face of the pressures of having to deal with competing species species-level selection is likely to be even more important. If DGDSWDWLRQLVWRKDYHDQLQÀXHQFHRQSRSXODWLRQ densities, then this could also change the behaviour, as selection pressures should differ between low and high density populations (chapter 2).

7KLV PHDQV WKDW WKHUH LV DOZD\V D SRWHQWLDO IRU a feedback between individual selection, and population ecology (Dieckmann & Metz 2006).

7KLVWKHVLVKDVVKRZQWKDWWKLVIHHGEDFNPD\EH an important factor limiting the intensity of con- ÀLFWVZHREVHUYHLQQDWXUHFKDSWHUDQGFKDSWHU 7KLV DORQJ ZLWK WKH IDFW WKDW WKH HYROXWLRQ RI LQWHQVH FRQÀLFWV PD\ UHVXOW LQ HYROXWLRQDU\

suicide, and may help to explain why we rarely REVHUYH H[DPSOHV RI VH[ DQG FRQÀLFW WKDW DUH extremely detrimental population processes.

7KH QDWXUDO ZRUOG PD\ QRW DSSHDU DV WUDJLF DV we might expect.

Acknowledgments

I thank Hanna Kokko, Sedeer El-Showk, Jostein Starrfelt and Emma Vitikainen , who all provided KHOSIXOFRPPHQWV7KHZULWLQJZDVIXQGHGE\WKH Academy of Finland.

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