Animal Ecology Evolutionary Biology Centre
Uppsala University
Relating life history and physiology
Kevin Fletcher
Introductory Research Essay No. 106 ISSN 1404 – 4919
Uppsala 2017
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Introductory Research Essay No. 106
Postgraduate studies in Biology with specialization in Animal Ecology
Relating life history and physiology
Kevin Fletcher
Department of Ecology and Genetics / Animal Ecology Evolutionary Biology Centre
Uppsala University Norbyvägen 18D SE-752 36 Uppsala
Sweden
ISSN 1404-4919
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ContentsIntroduction ………...4
The immune system ………...5
Innate and acquired immunity...5
Costs of immunity...7
The Hypothalamus pituitary adrenal axis ………...9
The fitness hypothesis...10
Glucocorticoid regulation...11
Linking Glucocorticoids and immunity ………...11
Glucocorticoids role in immune function...11
Preadaptation of Glucocorticoid and immune response...13
Conclusion ………...14
Acknowledgements ………...15
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IntroductionScience aspires to understand the complexity of life through simple explanations. Perhaps one of the most fascinating and complex areas of scientific study is life history evolution, which bids to
understand life cycle patterns, such as birth, death and reproduction in all living organisms1. Life history theory addresses how the principal life history traits (Table 1) combine in various ways to affect fitness, and central to the theory of life history are trade-offs. The most notable trade-offs are between current and future reproduction and current reproduction and survival2,3 , which are linked together by trade-offs between the said life history traits. The various combinations of traits gives some individuals advantages in reproduction and survival under certain conditions, and as far as those traits are heritable can result in evolutionary change. Thinking simply, physiological trade-offs occur when energy is favoured towards one trait over another from a finite resource, which is mediated by the endocrine system1. Adaptive variation is therefore constrained by limiting factors such as time and available nutrients for energy3.
Table 1. The principal life history traits that are fated together by various trade-offs (e.g. Age and size at maturity and age and size specific reproductive investment).
Principal Life history traits Size at birth
Growth pattern Size at maturity Age at maturity Number of offspring Size of offspring Offspring sex ratio Reproductive investment Mortality
Lifespan
A lot of life history variation comes from individuals responding to ecological conditions and stressful stimuli4. The resulting life history phenotypes are a consequence of the norms of reaction from a single genotype4. In other words, varied environmental conditions drives phenotype diversity. More recently, evolutionary biologists have started to address the matter of life histories in relation to physiological control mechanisms, which adapt the individual to the current environmental conditions1. Physiology encompasses all the normal mechanisms and interactions that make an
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organism function daily routines, which require energy and nutrition. During a particular period of an organisms’ life cycle, homeostatic mechanisms will balance the physiological system to support life, but when the life history stage changes, or, in response to unpredictable environmental fluctuations, the homeostatic balance must also change. This process is known as allostasis, and while
homeostasis explains the system that is required for life, allostasis explains those mechanisms responsible in maintaining life in balance, as an organism transitions through different life history stages, and responds to ecological conditions5,6.
There are many potential stressful events that threaten an organisms’ status quo, which result in both behavioural and physiological responses, in addition to the normal responses to the challenges of any given life stage. Potential stressful events include exposure to pathogens, inclement weather and low food availability. The effect that stress has on an organism and its’ subsequent response, will depend on the current life-history stage7,8. Here, two physiological systems, the immune function and endocrine control mechanism, are reviewed in relation to stress. Particular attention will be paid to the reproductive period of an organisms’ life cycle. The following are considered: Firstly, mounting an immune response requires resource that during reproduction will potentially be involved in trade- offs with life history traits9,10,11,12, secondly, the endocrine system, particularly the Hypothalamus Pituitary Adrenal axis, responds to stress by mediating the mobilization of resource to levels that either favour an organisms self-maintenance13,14, or, reproductive investment15,16. Finally, that these two systems are linked and when considered together can improve our understanding of life-history evolution. For the sake of this essay stress will refer to an event that evokes behavioural and
physiological responses, in order to recover from, or, avoid a threatening event.
The immune system
Innate and acquired immunity
Exposure to pathogens is an inevitability for the majority of organisms’, furthermore, the complexity of the vertebrate immune system is testament to the astonishing variety of pathogens that exist.
Vertebrates have evolved numerous adaptations to prevent pathogens from gaining access to their resource, to fuel their own reproduction, which is largely controlled by the innate and acquired immune system (Fig. 1). The innate response, also known as the non-specific response, is made up of many constitutive components that embody the first line of immune defence. The components of the innate response are found at low levels in the blood, meaning that they can be deployed quickly in response to a pathogen17. Macrophages, an important part of the innate system, recruite white blood cells, but also directly ingest pathogens whilst being essential in organizing the immune
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response18. Natural killer (NK) cells eliminate infected host cells, and complement proteins form complexes that lyse pathogens, as well as marking them for phagocytosis17. Cytokines produced by the constitutive components can induce an inflammatory response, which through behavioural and physiological changes, makes the host a less favourable place for the parasite to proliferate19. The main aim of an inflammatory response is to return homeostasis to the infected area, allowing for the host to continue with daily routines20. A cell mediated response in vertebrates, consists mainly of T lymphocytes, which respond to a parasite infection through generalized mechanisms such as phagocytosis. Acquired immunity functions in two ways, firstly, the cell mediated response utilises T cells (Fig. 1) that recognize and eliminate pathogens, with a subset of these T-cells able to memorize pathogens21, secondly, the humoral response utilises B-cells and Th2 cells (Fig. 1) to recognize pathogens, and then B-cells are differentiated to produce antibodies that neutralize, or, mark the pathogen for elimination21.
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Figure 1. Vertebrate immune mechanisms. Adapted from Muehlenbein 201022.
Costs of immunity
The aforementioned components of the immune system, differ in how physiologically costly they can potentially be to the host20. It is considered that acquired cell mediated immunity is costly due to the rapid expansion, and the later diversification of T-cells that requires nutrients and time. Pro-
inflammatory cytokines are produced by constitutive components of the innate immune system, as well as the acquired cell mediated components. Consequently, both innate and acquired immunity
Vertebrate immune mechanisms
Innate Acquired
(adapted)
Inflammatory response
Anatomical barriers resident
Interferon, heatshock proteins
Complement system
Macrophages,
neutrophils, NK cells…
Lymphocytes
B cells (humoral/antibody)
T cells (cellular immunity)
Immunoglobulins Cytotoxic Helper
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have the potential to induce an inflammatory response, the cost of which is currently undefined20. However, an inflammatory response causes change in metabolism, decreases level of activity, increases production of acute phase proteins (function in pathogen clearance), and initiates fever, all of which have undoubted costs to the host23,24. Humoral immunity is considered to be less costly, because it produces anti-inflammatory cytokines. Although most of the lymphocyte preparation is done at the development stage and requires substantial nutrients and time20. The responsiveness of the immune system to a pathogen depends on the current life history stage. During energy
demanding life stages such as reproduction, immune function is probably reduced, as more of the available resource is used to reproduce successfully2526.
Life history theory asserts that organisms are adapted to optimally allocate resource between fitness components, and that these trade-offs constrain adaptation3. The costs associated with mounting an immune response will undoubtedly come at a cost to the aforementioned fitness components10,9,27,28. Trade-offs involving immune function, termed the cost of immunity11, encompass the costs related to the evolution, maintenance and deployment of immune defence. Studies using insects have showed that selecting for better immunity comes at a cost to life-history traits. For example, it was found that an increase from 15% to 70% in resistance to a pathogen, negatively covaried with lifespan and offspring quality in Drosophila Melanogaster29. Similar results were shown in bumble bee colonies, were a negative covariance was found between susceptibility to pathogens and colony productivity30, additionally in crickets, the cost of immunity was found to be negatively associated with fitness31. These results show a negative correlation between immune function and other life history traits, which suggests that there is a negative cost to evolving heightened immune function.
Maintaining the immune system at a state of readiness, in anticipation of a pathogen invasion is costly, which should be detectable even in the absence of a pathogen. In mosquitoes a negative correlation was found between development time and immune responsiveness32. A negative
relationship between parasite resistance and fecundity, was also found in Drosophila in the absence of parasites33. This indicates that under certain environmental conditions, down regulation of immune responsiveness, might be required to maximise other traits that favour fitness. The
deployment of the immune defence can carry genetic costs as a consequence of specific genotypes, which becomes evident when various genotypes experience the same ecological conditions.
The physiological cost related to immune deployment is the plastic response to a pathogen. This is consequential of the host’s decision to either, invest in immune defence, or, other costly activities.
Evidence for this has come from studies that challenge the immune system during energy demanding life stages, which have identified a loss in fitness in response to an immune challenge. An experiment
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that quantified the encapsulation response to a foreign object in bees, showed that foraging bees that are required to fly in search of food, had lower encapsulation rates than stay at home bees that are less energy challenged34. Further, a study that immunized wild passerines with a novel vaccine, showed a negative correlation between reproductive effort and the vaccine specific antibodies in the following breeding season35. Additionally, birds that were assigned to the larger brood treatment and harboured haemosporidian parasites, were found to have higher parasiteamia (infection intensity)35. This indicates that the birds favoured reproduction over immunity, whereby a physiological trade-off was made between immunity and reproductive effort.
The Hypothalamus pituitary adrenal axis
The endocrine system controls physiological and behavioural responses to unpredictable
environmental events, and also to predictable events such as reproduction6,36,37,38. Glucocorticoids (GCs) are steroid hormones that are essential in the mobilization of stored non-carbohydrate energy, along with regulating glucose levels to fuel behaviours39. As well as being important in stress
response, GCs are known to regulate the annual cycle6. Furthermore, the baseline level of GCs during reproduction has been associated with reproductive success and thus has the potential to provide important insights into the important link between physiology and life history. GC level in the blood is controlled by the HPA axis, a cascade of 3 glands that stimulate each other, and also feedback to prevent excessive GCs being produced (Fig. 2)39. Prolonged acute levels of GCs can have negative consequences, which can result in an individual halting any costly behaviours, and entering into what is known as the emergency life history stage13. This is when an individual favours self-maintenance over costly behaviours such as reproduction. However, the up-/down-regulation of GCs within normal limits, initiates many metabolic pathways and behaviours and is thus essential for maintaining homeostasis40.
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Figure 2. The Hypothalamus pituitary adrenal axis. Stimulation of the hypothalamus results in the production of CRH which stimulates the anterior pituitary gland to produce ACTH. Then ACTH stimulates the adrenal cortex to produce GCs. GCs then initiate many metabolic pathways, but also function as a negative feedback on the Hypothalamus and anterior pituitary gland.
Glucocorticoids and life history
The fitness hypothesis
The fitness hypothesis is usually referred to as the cort-fitness hypothesis, because corticosterone is the principal GC in birds and most studies of this nature focus on birds. The upregulation of GCs in response to environmental conditions is what forms the basis of the cort-fitness hypothesis41. It is expected that elevated GC levels are associated with redirecting resource away from costly activities such as reproduction, which will inevitably have a negative impact on fitness. Further, to the extent that baseline GC level is heritable and has an effect on phenotypic traits, stress related elevated GC levels, in response to challenging conditions, could indicate poor quality individuals41. Finally, acute stress levels of GCs and their direct effect on fitness, explain the predicted negative relationship between GCs and fitness41. Together these predictions suggest that baseline GCs elevate in response to an environmental challenge, and that fitness declines as conditions worsen. This results in a negative relationship between baseline GCs and fitness. A review found a negative relationship between baseline GC and fitness, in only half of the studies that tested this relationship41. This means that other factors must be considered to understand the relationship between baseline GCs and fitness.
Hypothalamus
Anterior Pituitary Gland
Adrenal cortex
Corticotropin releasing hormone (CRH)
Adrenocorticotropic hormone (ACTH)
Glucocorticoid (GC)
Negative feedback
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Glucocorticoid regulationThe GC level in the blood is fluctuating, so when the sample is taken could potentially affect the baseline GC level detected42. Further, a number of studies in birds have found that baseline GC levels change, as an individual progresses through the different stages of the breeding season6,43,44,45,46. Lower GC levels have generally been detected early in the breeding season, and later during the nestling feeding period, GC levels are generally found to be higher. This could be a consequence of the increased energy demands associated with providing care 47,48,49. Moreover, it was found that house sparrows (Passer domesticus) with low baseline GC levels during pre-breeding, and higher levels during nestling feeding fledged more offspring. This indicates that the plasticity of the GC response during reproduction, is crucial for reproductive success43. Many studies relate fitness to a single measurement of GC. A better method would be to build up a baseline GC profile of each individual, by taking several samples over the period of reproduction. This would then account for the normal changes in baseline GCs, in response to the different challenges of each stage of reproduction. The measure of fitness used should also be considered, as many studies opt for an annual measure of fitness, due to the difficulty in identifying more extensive fitness measures e.g. life time reproductive success. A case in point, is a study that used an integrated measure of fitness (number of offspring produced over several years) in albatrosses. It was found that higher levels of baseline cort during the breeding period, were indeed negatively associated with fitness50. It is also worth noting that baseline cort might be adapted to different conditions between populations, and also within regions of what is considered a continuous population. Caution should therefore be taken, when attempting to find a single cort phenotype that best adapts organisms to unpredictable conditions, because like with all theories related to life history evolution, the answer is likely to be much more complicated.
Linking glucocorticoids and immunity Glucocorticoids role in immune function
It is predicted that in response to stress, immune function is involved in a resource trade-off were immunity is reduced, so that resources can be reallocated to behaviours that directly improve survival chances51. The HPA-axis hormones have both influencing and inhibiting effects on a wide range of immunity components52, which means that the activation and strength of the stress
response, can influence the immune response to a pathogen. The main function of glucocorticoids in immunity, is to inhibit the production and release of cytokines that initiate immune and
inflammatory responses53,54. They can affect the expression level of MHC II proteins by inhibiting
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antigen presentation. In addition, they can halt the proliferation of T-and B-cells and promote the production of anti-inflammatory proteins by Th2, while slowing the production of pro-inflammatory proteins by Th155,56,57. GCs can lower circulating lymphocytes and alter the movement and function of peripheral cells, leading to a reduction of lymphocytes, macrophages and monocytes, which are suppressed at inflammatory sites when reducing the accumulation of phagocytes58,59.
Early predictions of the homeostatic role of GCs in immunosuppression, included making more energy available for other more crucial functions, and that GC induced lymphocytosis could indeed provide energy for competing resource dependent traits 51. In addition to the above mentioned predictions is the autoimmune hypothesis, which suggests that GCs work to select the components of the immune response to reduce the chance of autoimmunity. When a pathogen challenges the immune system it induces a polyclonal response, which comes with a risk, because the antigenic determinants recognised by some of the clones might crossover over with those of self-cells51. GCs inhibit auto-immune prone or redundant components of the immune system and thus reduce the risk of autoimmunity 60.
More recently, it has become recognised that GCs may assist immunity by enhancing the production of immunoglobulins by cultured B-cells61,62,63, enhance T-cell function64 along with directing the movement of leukocytes to areas of infection65,66,67. The acute phase response, which is mainly an innate immune response to infection or injury, is both enhanced and suppressed by GCs. GCs increase the sensitivity of mediators of acute phase proteins, and complement components
synthesis, as well as inhibit the mediators to suppress the overall response68,69. The action of the GCs early on in the immune response is to enhance and can be considered permissive, whereas later on in the immune response, it works to inhibit those same processes and becomes an immune
suppressor51. The function of GCs in immune response seems to vary with the length and severity of the stressful event. During the early phase of a stressful event, GCs seem to work to enhance predominantly innate immunity then later acquired immunity, but if the stressful event is prolonged GCs can then also suppress both responses (Fig. 3)70. It is worthy of note that the innate immunity trajectory starts at a higher level of immune function (Fig. 3). This is because the constitutive components of the innate immune system are already present at low levels in the blood.
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Figure 3. How different immune functions (innate -black dotted line, acquired- solid line) in domestic rodents progress related to stress duration. Glucocorticoids are the main mediator of immune change, although others mediators such as SNS-derived peptides are also important. Adapted from Martin 200971
Preadaptation of Glucocorticoid and immune response
How an individual responds to stress may be a consequence of preadaptation. It is evident that, the level of stress experienced during early development, can indeed influence how one responds to stressful situations in adulthood72,73,74,75. For example, food deprived western scrub-jay nestlings (Aphelocoma californica), were found to have a stronger response to stress at 12 months old than nestlings fed a nutritious diet76. This might indicate that stress experienced during early
development, predetermines the GC stress response later in life. In addition, elevated baseline levels of GCs experienced during early development, has been shown to increase the sensitivity of
leukocytes to elevated levels of GCs later in life77. Given that mothers can pass on GCs in ovo or in utero, in an adaptive sense, the level of exposure to GCs during early development, might be linked to the likelihood of encountering stressful events in adulthood. The immune system is therefore preadapted to probable future conditions70. A study monitoring Florida scrub jays (Aphelocoma
Minutes-hours Hours-days Days-weeks Weeks-months
Immune funct io n
Time to effectiveness
Glucocorticoids
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coerulescens), revealed a negative correlation between the time adult birds spent by the nest and the level of nestling baseline GCs78. The parental care provided by the parents might be related to their condition, or, the perceived risk of predation. Thus, the level of baseline GCs experienced during early development, is linked to the environment experienced by the parents, which might indirectly preadapt the nestlings to that environment.
Conclusion
The variety of life history strategies can in part be attributed to physiological adaptations that have a direct effect on survival and fitness. Studies have clearly showed that there are fitness costs to immunity. For example, genetic costs of immunity can come about when alleles code for enzymes, that don’t function optimally under the current conditions. On the other hand, the physiological costs of immunity are involved in trade-offs, where the deployment of the immune defence, is reduced in favour of other fitness traits that influence successful reproduction. However, the costs related to maturing and preparing the immune system remains largely undetermined. Glucocorticoid steroid hormones have wide ranging functions. Recently studies have showed, that the up and down regulation of GCs during reproduction, has important fitness and survival consequences. The
complexity of the immune system alone, makes identifying the cost of immunity on fitness difficult to study. Thus, trying to incorporate the role of glucocorticoids into the relationship between immune defence and fitness, only further complicates the matter. Current hypotheses predict that GCs act to suppress the immune system in response to stress. However, this is unlikley to be the complete picture, because certain stressful events will indeed require an active immune response. Instead, a more likely explanation is that in response to stress, GCs function initially as immune enhancers.
Then if the stress doesn’t subside, GCs become immune suppressors to prevent negative
consequences e.g. autoimmunity. Finally, both GCs and immunity are limited in how they function by the current environmental conditions. Furthermore, conditions during early development can influence the baseline GC level, which in turn stimulates the immune system. Early studies have showed, that these early interactions between GCs and parts of the immune system, can
predetermine how the immune system responds to stress in adulthood. It is clear that to improve our understanding of life history evolution, more attention must be given to how the interaction of such physiological mechanisms affects fitness and survival.
Acknowledgements
Thanks to all who have inspired, stimulated and motivated me in one way or another.
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19
ESSAYS IN THE SERIES ISSN 1404-4919
1. Reproductive patterns in marine animals on shallow bottoms. - Anne-Marie Edlund.
1979
2. Production in estuaries and saltmarshes. - Staffan Thorman. 1979 3. The evolution of life history traits. - Anders Berglund. 1979
4. Predation in marine littoral communities. - Carin Magnhagen. 1979
5. Insular biogeographic theory, developments in the past decade. - Stefan Ås. 1979 6. Theories and tests of optimal diets. - Juan Moreno. 1979
7. Ecological characters in insular communities. - Mats Malmquist. 1980 8. Plant/insect relationships: a synopsis. - Ola Jennersten. 1980
9. Sexual size dimorphism in birds of prey. - Per Widén. 1980 10. The evolution of avian mating systems. - Per Angelstam. 1980
11. Dispersal, dispersion and distribution in small rodent populations. - Fredric Karlsson.
1980
12. Age-related differences of competence in birds. - Karin Ståhlbrandt. 1980 13. Respiration measurements as a tool in fish ecology. - Bengt Fladvad. 1981 14. Intraspecific variation; its adaptive value and consequences. - Lars Gustafsson.
1981
15. Cooperative breeding in birds: theories and facts. - Mats Björklund. 1982 16. Some aspects of parasitism. - Göran Sundmark. 1982
17. Evolution and ecology of migration and dispersal. - Jan Bengtsson. 1982 18. Are animals lazy? - Time budgets in ecology. - Bodil Enoksson. 1983 19. Ecology of island colonization. - Torbjörn Ebenhard. 1983
20. Reproductive habits and parental care in some lacustrine African Cichlids (Pisces) with special reference to Lake Malawi species. - Ulrich Jessen. 1983
21. Monogamy or polygyny? - Mating systems in passerine birds. - Björn Westman.
1983
22. Distributional patterns in reptiles and amphibians. - Per Sjögren. 1983 23. Some theoretical considerations of dispersal. - Gunnar Nilsson. 1983 24. Interactions between animals and seeds. - Urban Wästljung. 1984
25. Reproductive modes and parental care in fishes. - Ingrid Svensson. 1984 26. Reproductive strategies in fishes. - Peter Karås. 1984
27. Sexual selection and female choice based on male genetic qualities. - Jacob Höglund. 1984
28. The timing of breeding in birds with special reference to the proximate control. - Mats Lindén. 1985
29. Philopatry and inbreeding versus dispersal and outbreeding. - Tomas Pärt. 1985
30. Evolution of sociality in Hymenoptera. - Folke Larsson. 1985
20
31. Bird song and sexual selection. - Dag Eriksson. 1986 32. The energetics of avian breeding. - Lars Hillström. 1986 33. Sex role reversal in animals. - Gunilla Rosenqvist. 1986
34. Factors affecting post-fledging survival in birds. - Kjell Larsson. 1986
35. Quantitative genetics in evolutionary ecology: methods and applications. - Pär Forslund. 1986
36. Body size variations in small mammals. - Anders Forsman. 1986
37. Habitat heterogeneity and landscape fragmentation - consequences for the dynamics of populations. - Henrik Andrén. 1986
38. The evolution of predispersal seed predation systems in insects. - Mats W.
Pettersson. 1987
39. Animal aggregations. - Anette Baur. 1988
40. Operational and other sex ratios: consequences for reproductive behaviour, mating systems and sexual selection in birds. - Jan Sundberg. 1988
41. Genetic variation in natural populations. - Annika Robertson. 1989 42. Adaptations for a parasitic way of life. - Reija Dufva. 1989
43. Predator-prey coevolution. - Lars Erik Lindell. 1990 44. Parasite impact on host biology. - Klas Allander. 1990
45. Ecological factors determining the geographical distribution of animal populations. - Berit Martinsson. 1990
46. Mate choice - mechanisms and decision rules. - Elisabet Forsgren. 1990
47. Sexual selection and mate choice with reference to lekking behaviour. - Fredrik Widemo. 1991
48. Nest predation and nest type in passerine birds. Karin Olsson. 1991
49. Sexual selection, costs of reproduction and operational sex ratio. - Charlotta Kvarnemo. 1991
50. Evolutionary constraints. - Juha Merilä. 1991 51. Variability in the mating systems of parasitic birds.
Phoebe Barnard. 1993.
ISRN UU-ZEK-IRE--51—SE52. Foraging theory: static and dynamic optimization.
Mats Eriksson. 1993.
ISRN UU-ZEK-IRE--52—SE53. Moult patterns in passerine bird species.
Christer Larsson. 1993.
ISRN UU-ZEK-IRE--53--SE54. Intraspecific variation in mammalian mating systems.
Cheryl Jones. 1993.
ISRN UU-ZEK-IRE--54--SE55. The Evolution of Colour Patterns in Birds.
Anna Qvarnström. 1993.
ISRN UU-ZEK-IRE--55--SE56. Habitat fragmentation and connectivity.
Torbjörn Nilsson. 1993.
ISRN UU-ZEK-IRE--56—SE57. Sexual Selection. Models, Constraints and Measures.
David Stenström. 1994.
ISRN UU-ZEK-IRE--57—SE21
58. Cultural Transmission and the Formation of Traditions in Animals.
Henk van der Jeugd. 1995.
ISRN UU-ZEK-IRE--58—SE59. Ecological Factors Affecting the Maintenance of Colour Polymorphism.
Sami Merilaita. 1995.
ISRN UU-ZEK-IRE--59—SE60. The Evolution and Maintenance of Hermaphroditism in Animals.
Anna Karlsson. 1996
. ISRN UU-ZEK-IRE--60—SE61. Costs and Benefits of Coloniality in Birds.
Tomas Johansson.
1996. ISRN UU-ZEK-IRE--61—SE62. Nutrient reserve dynamics in birds.
Måns S. Andersson. 1996.
ISRN UU-ZEK-IRE--62—SE
63. Nest-building for parental care, mate choice and protection in fishes.
Sara Östlund. 1996.
ISRN UU-ZEK-IRE--63—SE64. Immunological ecology.
Dag Nordling. 1996.
ISRN UU-ZEK-IRE--64—SE65. Hybrid zones and speciation by reinforcement.
Anders Ödeen. 1996.
ISRN UU-ZEK-IRE--65—SE66. The timing of breeding onset in temperate zone birds.
Robert Przybylo. 1996.
ISRN UU-ZEK-IRE--66—SE67. Founder speciation - a reasonable scenario or a highly unlikely event?
Ann-Britt Florin. 1997. I
SRN UU-ZEK-IRE--67—SE68. Effects of the Social System on Genetic Structure in Mammal Populations.
Göran Spong. 1997.
ISRN UU-ZEK-IRE--68—SE69. Male Emancipation and Mating Systems in Birds.
Lisa Shorey. 1998.
ISRN UU-ZEK-IRE--69—SE70. Social behaviours as constraints in mate choice.
Maria Sandvik. 1998.
ISRN UU-ZEK-IRE--70—SE71. Social monogamy in birds.
Kalev Rattiste. 1999.
ISRN UU-ZEK-IRE--71--SE72. Ecological determinants of effective population size.
Eevi Karvonen. 2000.
ISRN UU-ZEK-IRE--72—SE73. Ecology of animals in ephemeral habitats.
Jonas Victorsson. 2001.
ISRN UU-ZEK-IRE--73--SE74. Extra-pair paternity in monogamous birds.
Katherine Thuman. 2001.
ISRN UU-ZEK-IRE--74-SE75. Intersexual communication in fish.
Niclas Kolm. 2001.
ISRN UU-ZEK-IRE--75—SE76. The role of postmating prezygotic reproductive isolation in speciation.
Claudia Fricke. 2002.
ISRN UU-ZEK-IRE--76—SE77. Host parasite interactions: Local adaptation of parasites and changes in host behaviour. - Lena Sivars. 2002.
ISRN UU-ZEK-IRE--77—SE78.
