Competition, Coexistence and Character Displacement: in A

List of Papers

This thesis is based on the following papers, which are referred to in the text by their Roman numerals.

I Vallin, N., Rice, A. M., Arntsen, H., Kulma, K. and Qvarn- ström, A. (2011) Combined effects of interspecific competition and hybridization impede local coexistence of Ficedula flycatchers. Submitted manuscript.

II Qvarnström, A., Wiley, C., Svedin, N. and Vallin, N. (2009) Life-history divergence facilitates regional coexistence of competing Ficedula flycatchers. Ecology 90:1948-1957.

III Vallin, N., Nonaka, Y., Feng, J. and Qvarnström, A. (2011) Life-history divergence and environmentally dependent relative fitness of hybrid nestlings in Ficedula flycatchers. Manuscript.

IV Vallin, N., Rice, A. M., Bailey, R. I., Husby, A. and Qvarn- ström, A. (2011) Positive feedback between ecological and reproductive character displacement in a young avian hybrid zone. Submitted manuscript.

V Vallin, N. and Qvarnström, A. (2011) Learning the hard way: imprinting can enhance enforced shifts in habitat choice. Sub- mitted manuscript.

Reprints were made with permission from the publisher.

Cover picture: variation in male pied flycatcher plumage coloration. Artwork by Måns Hjernquist.

Contents

1. Introduction ...... 7 2. Study system ...... 10 The Ficedula flycatcher hybrid zone on Öland ...... 10 3. Aims of the thesis...... 13 3.1. The interaction between competition and hybridization in causing local extinction ...... 13 3.2. The role of life history divergence in facilitating regional coexistence ...... 15 3.3. The role of life history divergence for the relative fitness of hybrids across different environmental conditions ...... 17 3.4. The interplay between ecological and reproductive character displacement ...... 19 3.5. The role of early learning in causing shifts in habitat choice ...... 21 4. Conclusions and future perspectives ...... 23 4.1. Competition and coexistence ...... 23 4.3. Evolutionary implications ...... 24 5. Sammanfattning på svenska ...... 26 6. Acknowledgements ...... 31 7. References ...... 33

1. Introduction

Since Darwin (1859), the definition of species has shifted from being based on morphological differences between them towards a definition based on reproductive isolation, i.e. the degree of reduced interbreeding between them through different isolating barriers (Dobzhansky 1937, Mayr 1942). Howev- er, Darwin’s (1859) general ideas on the importance of natural selection for the origin of species have gained increasing support and attention in recent years (Schluter 2000, Coyne and Orr 2004, Price 2007). The evolution of reproductive isolation through ecologically based divergent selection is commonly referred to as ecological speciation (Schluter 2001, Rundle and Nosil 2005), and predicts that reproductive isolation should evolve between populations when adapting to contrasting environments but not between populations when adapting to similar environments (Schluter 2009). Reproductive isolation comes in many forms, which fall into two main categories; prezygotic and postzygotic. Prezygotic isolation acts before ferti- lization and can be ecological (e.g. habitat or temporal isolation), behavioral (e.g. divergence in mate preferences), mechanical (e.g. incompatibilities in reproductive structures), or gametic (e.g. incompatibilities between ga- metes). Postzygotic isolation acts through reduced fitness of hybrids, and can be further divided into extrinsic (e.g. hybrids are unable to find an ecological niche and/or to obtain a mate) and intrinsic (e.g. hybrids are inviable or sterile) forms (Coyne and Orr 2004). To what extent intrinsic postzygotic isolation in terms of genetic incompatibilities between populations (e.g. the “Dobzhansky-Muller” model, Dobzhansky 1937, Muller 1942) arise as a result of adaptation remains an open question (Coyne and Orr 2004). By contrast, extrinsic postzygotic isolation is often a direct result of adaptive evolution (Hatfield and Schluter 1999). Hybrids are often phenotypically intermediate between pure species, and may therefore be unfit in either parental habitat (reviewed in Coyne and Orr 2004). Hybrids may also be intermediate in behavior, as in the hybrids between two populations of blackcaps who undertake an intermediate migratory route as compared to the parental populations (Helbig 1991). Behavioral sterility is another form of extrinsic hybrid inviability where hybrids are rejected by potential mates due to their intermediate phenotype.

Allopatric speciation appears to be a non-controversial mode of speciation. Given enough time apart, pairs of isolated taxa are likely to evolve reproduc-

7 tive barriers. However, sooner or later, these pairs are also likely to experience secondary contact with each other. The topic of coexistence between similar species has fascinated the scientific community for decades (Volterra 1926, Lotka 1932, Gause 1934, Hardin 1960, Kuno 1992, Gröning and Hochkirch 2008). Can closely related species coexist in the same habitat, and if so - how? How important are interactions such as competition and hybridization between species in driving speciation events or extinctions? These types of questions are more relevant today than ever as global environmental changes are increasingly affecting species distributions and diver- sity in a number of direct and indirect ways. Climate change, translocations, and habitat disturbance are expected to increase the prevalence of biological invaders (Sala et al. 2000), which in turn will increase the probability for hybridization and competition between formerly separated closely related species. There are already several examples of hybridization driving species to extinction (Rhymer and Simberloff 1996), but replacement of species and hybridization are often treated as independent subjects in conservation biology (Konishi and Takata 2004). By contrast, there is also a more positive viewpoint on hybridization and biodiversity. For example, hybridization can be seen as a natural process with the potential to genetically enrich rare species (Arnold 1997), as a source for rapid adaptive diversification (Lewontin and Birch 1966, Seehau- sen 2004), and as a means to facilitate microevolutionary changes in response to climatic extremes (Grant and Grant 1993). Secondary contact between closely related species is “revitalizing the ghosts of competition and evolution” (Confer 2006), and is generally considered to result in either the extinction of one population, stable coexistence with hybridization, or for- mation of distinct species by the buildup of reproductive isolation and niche separation (Liou and Price 1994).

When the enhancement of reproductive isolation in sympatry is driven by natural selection against hybridization the process is referred to as reinforcement (Dobzhansky 1940). As reinforcement might be an important process in finalizing speciation, it has received considerable empirical and theoretical attention (reviewed by Servedio and Noor 2003). One of the major criticisms against reinforcement is that it can only work under a rather narrow window of conditions: hybridization must be fairly common to exert a significant selection pressure (Moore 1957), but not so prevalent that re- combination breaks down the association between genes influencing hybrid fitness and genes coding for traits important for assortative mating (Barton and Hewitt 1985). According to the advocates of reinforcement (see Serve- dio and Noor 2003 and references therein), the process of reinforcement, i.e. selection to avoid hybridization, can lead to a pattern of divergent resource- use or reproductive phenotypes between populations.

8 However, divergence in resource-use or in reproductive phenotypes, i.e. character displacement (Brown and Wilson 1956), can also reduce other harmful interactions between populations. Ecological character displacement (evolution resulting from selection to reduce interspecific resource competition) and reproductive character displacement (evolution resulting from selection to minimize interspecific reproductive interference) can result in a pattern of geographical variation where populations in sympatry with a closely related heterospecific differ from conspecific populations in allopatry. One difficulty with inferring process from pattern is that character displacement driven by competition could create a similar pattern of greater divergence in sympatry than in allopatry as character displacement through reinforcement would. Hence, reinforcement could also be seen rather as a special case of the process of reproductive character displacement (Blair 1974, Pfennig and Pfennig 2009). Increasing support for the importance of interspecific aggression in causing selection on secondary sexual characters is accumulating (Butcher and Rohwer 1989, Seehausen and Schluter 2004, Tynkkynen et al. 2004, 2005, Grether et al. 2009, Anderson and Grether 2010), and an evolutionary response to competition over resources may lead to reproductive isolation as a by-product, e.g. through displacement in habitat choice (e.g. Feder et al. 1994, Schluter 2000) or breeding time (Théron and Combes1995, Hendry and Day 2005).

Despite the revitalized interest in the process of speciation over the last decades, and the recent revival of the potential importance of ecology in this process, few attempts have been put forward to adopt a holistic approach. Most studies aim to disentangle the relative importance of allopatric or sympatric divergence, or on the relative importance of different sources of selection in driving population divergence. The interactions between ecological and reproductive character displacement have rarely been studied, although closely related species that compete for resources are also likely to interact during mate acquisition (Pfennig and Pfennig 2009). In this thesis I combine experimental and empirical data from a long-term study in a young hybrid zone to investigate the ecological and evolutionary implications of secondary contact between two closely related bird species, pied (Ficedula hypoleuca) and collared (F. albicollis) flycatchers.

9 2. Study system

The Ficedula flycatcher hybrid zone on Öland

Pied and collared flycatchers co-occur in a large hybrid zone in central and eastern Europe, as well as in a more isolated hybrid zone across the Baltic isles of Öland and Gotland in Sweden. The studies of this thesis have been conducted on Öland. On Öland (57°10´N, 16° 58´E), approximately 2000 nestboxes are monitored annually in 21 different areas scattered across the island. One of the areas was monitored already in the years 1981-1985, but the current large- scale study was initiated in 2001-2002. The overall proportion of the species is approximately 80% collared flycatchers, 15% pied flycatchers and 5% of heterospecific pairs. Collared flycatchers started to colonize Öland, where pied flycatchers were already present, in the late 1950’s-early 1960’s around the town of Löttorp in the north of the island. Löttorp and its surroundings now harbor the highest densities of collared flycatchers. The relative proportion of collared flycatchers gradually declines southward, and, more abrupt- ly, northwards (Fig. 1). The landscape on Öland is characterized by a mix- ture of agricultural land and rich deciduous forest, except for the very nor- thernmost part of the island, which also contains areas dominated by coniferous forest. The males start arriving at the breeding grounds in late April and imme- diately begin to compete for natural breeding holes or nest-boxes (Alatalo et al. 1994, Pärt and Qvarnström 1997, Qvarnström 1997). Male pied and collared flycatchers differ both in song and plumage traits (Svensson 1992). Males of both species generally exhibit a black and white plumage, but male collared flycatchers are slightly bigger (with longer wings and tail) than male pied flycatchers, and collared flycatchers also have more pronounced white patches on the wings and on the forehead (Fig. 2). The plumage of male pied flycatchers is more variable, and ranges from black and white to female-like brown and white (see cover and paper IV). The females of the two species are more similar to each other. However, female collared flycatchers are slightly bigger and more grey in color (female pied flycatchers are more brown), have larger white patches on their wings and a rudimentary white color hidden at the base of the feathers on the neck (Svensson 1992). The two species are also easily separated by species-specific alarm calls. Male

10 hybrids are identified through their intermediate plumage pattern and female hybrids through their complete sterility. Later generation backcrosses are extremely rare due to accumulated costs of hybridization (Wiley et al. 2009).

Löttorp area ~130 km

CF MIX PF

Figure 1. Relative proportions of pied flycatchers (PF), collared flycatchers (CF), and heterospecific pairs (MIX) on the Swedish island of Öland in the years 2002- 2009. “Löttorp area” refers to the most densely populated study plots surrounding the town of Löttorp where collared flycatchers started to colonize the island in the 1960’s.

As a standard field procedure, all birds are individually marked with num- bered metal rings and detailed yearly records on onset of breeding and reproductive success are kept. Birds are caught once every breeding season with a trap inside the nest-box (or occasionally with a net), to enable blood sampling and measurements of morphological characters. Females are caught during incubation, and males when feeding nestlings. Nestlings are measured at day 7 and 13, and the nest-box is visited a couple of days after expected fledging to achieve an accurate estimate of breeding success.

Figure 2. A male collared flycatcher (Ficedula albicollis) displaying large white ornaments as he delivers newly caught prey to the nest. Photo by Johan Träff.

12 3. Aims of the thesis

In this thesis I explore the following topics:

1. The interaction between competition and hybridization in causing local extinction (Paper I)

2. The role of life history divergence in facilitating regional coexistence (Paper II)

3. The role of life history divergence for the relative fitness of hybrids across different environmental conditions (Paper III)

4. The interplay between ecological and reproductive character displacement (Paper IV)

5. The role of early learning in causing shifts in habitat choice (Paper V)

A summary of the main findings is given below.

3.1. The interaction between competition and hybridization in causing local extinction

Simulation models suggest that hybridization increases the risk of extinction beyond the risk resulting solely from competition (e.g. Wolf et al. 2001), but the importance of hybridization (or other forms of reproductive interference) in driving species replacements has been largely neglected (Gröning and Hochkirch 2008). We investigated the effects of hybridization, interspecific male competition over nest sites and over food used for reproduction on the population dynamics of pied and collared flycatchers breeding on the island of Öland, Sweden. Collared flycatchers started to colonize Öland in the late 1950’s-early 1960’s around the town of Löttorp in the north of the island where they now breed in high densities (Fig. 1). Nest-box areas surrounding Löttorp were selected to study how a rapid increase in the number of breed-

13 ing collared flycatchers has affected pied flycatchers in terms of reproductive success, lifespan and pairing patterns.

The forests in this area are dominated by deciduous trees such as Hazel (Co- rylus avellana), Oak (Quercus sp.) and Ash (Fraxinus excelsior), known to provide a high abundance of prey suitable for flycatchers (i.e. caterpillars), although during a relatively short period of time (e.g. Veen et al. 2010). Pied flycatchers were almost as common as collared flycatchers in this area as late as in the early 1980’s (see paper II), but are now approaching local extinction (Fig. 3). In paper I we show that one factor contributing to the rapid decline of pied flycatchers is the inability of young male pied flycatchers to establish territories with increasing numbers of breeding collared flycatchers. We found no differences in average reproductive success or reproductive lifespan between the two species, indicating that male pied flycatchers that have managed to establish themselves in the area are equally efficient at utilizing the available resources as male collared flycatchers. Neither did we find any trends of pied flycatchers declining on the Swedish mainland (where collared flycatchers are absent) or in the areas on Öland where collared flycatchers are absent.

70 137 154 201 138 202 197 211 1.00

0.75

0.50

0.25 CF males Proportion of males of Proportion PF males 0.00 2002 2003 2004 2005 2006 2007 2008 2009

Study year

Figure 3. The proportion of male pied flycatchers (“PF”, filled bars) has declined significantly in recent years within the area where collared flycatchers (“CF”, empty bars) colonized the Swedish Baltic island of Öland in the 1960’s. Sample sizes are given above the bars.

Is a lower competitive ability of young male pied flycatchers enough to ex- plain the rapid decline of pied flycatchers observed in this area? To answer this we also investigated the pairing patterns of female pied flycatchers. Fe- male pied flycatchers also declined in numbers across the study period, but less pronounced, compared to the male decline, and with a slight time lag

14 behind the males. This sex biased exclusion led to a steady increase in the proportion of hybridizing female pied flycatchers (Fig. 4). As hybridization is associated with large costs in flycatchers (a fitness reduction of approximately 97%, Wiley et al. 2009), the main negative effect of hybridization is lost reproductive opportunity. At the end of the study period in paper I, a majority of the female pied flycatchers paired with a male collared flycatcher, which is bound to speed up the local exclusion of pied flycatchers. Our results in this study highlight the importance of considering the combined effects of competition and hybridization when interpreting the population dynamics of closely related species experiencing secondary contact.

15 311218 10 21 17 11 1.00

0.75

0.50

0.25 CF males Proportion of males of Proportion PF males 0.00 2002 2003 2004 2005 2006 2007 2008 2009

Study year

Figure 4. Pairing patterns of female pied flycatchers in the areas where collared flycatchers breed in high density on the Swedish island of Öland. The proportion of female pied flycatchers that hybridize has increased across the study period, and in 2009 most of them paired with a heterospecific male (“CF”, open bars). Sample sizes are given above the bars.

3.2. The role of life history divergence in facilitating regional coexistence

Understanding species distributions is a major goal in ecological and evolutionary studies. Ecological similarity is traditionally considered to lead to competitive exclusion (Lotka 1932, Gause 1934, Hardin 1960), but similar species may be more likely to coexist if fluctuations in environmental conditions favor different species at different times or places (Chesson and Hunt- ley 1997, Amarasekare and Nisbet 2001). In paper II we were able to pin- point differences in life-history adaptations between pied and collared flycatchers that might prolong coexistence between these two otherwise very similar species.

15 We investigated how pied and collared flycatchers respond to changes in environmental conditions by partial cross-fostering of nestlings between the two species. Using this approach we were able to control for potential differences in microhabitat (i.e. location of the nest-box) as well as habitat use by the adult birds. In addition, the cross-fostering experiment was combined with a brood size manipulation where we either added two nestlings (to simulate a harsh environment) or removed two nestlings (to simulate a good environment) in the matched nests. Our results in paper II show that collared flycatchers have a relatively higher nestling mortality rate late in the breeding season compared to pied flycatchers (Fig. 5).

1 27 2 18 0.9 38 223 10 16 253

0.8 102 10

0.7 Pied Collared ----

0.6

Proportion Proportion of surviving nestlings -15 -10 -5 0 5 10 15

Timing of breeding

Figure 5. Nestling survival of pied and collared flycatchers in relation to timing of breeding (onset of egg laying corrected for the yearly mean). Nestling collared flycatchers experience a significantly higher mortality risk late in the season.

The cross-fostering experiment revealed that this difference in mortality is at least partly caused by intrinsic differences between the species. Collared flycatcher nestlings were significantly heavier than their pied flycatcher step- siblings at day 3. The mass gain from day 3 to day 12 of collared flycatchers was negatively related to the timing of breeding in nests with increased brood size, but not in nests with reduced brood size. This suggests that the smaller clutch size of collared flycatchers compared to pied flycatchers (Qvarnström et al. 2005) reflects an adaptive adjustment to their offspring’s higher sensitivity to lower food availability. However, we did not find any significant interaction between the treatment (brood size manipulation) and species of the nestling on growth. A possible reason for this could be that nestling collared flycatchers beg more intensively for food as compared to

16 nestling pied flycatchers, and are therefore more likely to be fed by the parents when sharing the same nest (Qvarnström et al. 2007). Why does a higher growth potential under favorable conditions lead to a higher mortality risk under poor conditions? The most obvious explanation is that a higher food demand is directly linked to a greater risk of starvation under poor conditions. Another potential explanation is that a higher food demand leads to more intensive begging, which may attract predators (Haskell 1994). In our experiment, the first explanation seems more likely as predation of complete broods is more common than partial predation of broods. We argue in paper II that this difference in environmentally dependent nestling mortality sets the stage for where and when the relatively more aggressive collared flycatchers are able to displace pied flycatchers, which will increase our chances of making predictions regarding the distributions of the two species across different types of environments.

3.3. The role of life history divergence for the relative fitness of hybrids across different environmental conditions

Paper III continues on the life-history theme introduced in paper II, but this time from the perspective of hybrids between the two flycatcher species. The possible fitness consequences of intermediate life history traits of hybrids have not received much scientific attention as compared to the problems associated with an intermediate morphology (Schluter 2000, Seehausen 2004, Parent et al. 2008). This is surprising because traits involved in reproduction are the ones that show the first signs of genetic incompatibility and may therefore play an important role early in the speciation process. Life- history traits have for example been shown to play an important role in local adaptations (Samietz et al. 2005, Jensen et al. 2008), and divergence in life- history traits could be of particular importance to local adaptation in phases where individuals are unable to escape suboptimal conditions, e.g. during the juvenile phase (Jensen et al. 2008). In paper III we investigated whether the observed life history divergence between pied and collared flycatchers cause environmentally dependent selection against nestling hybrids. We found that heterospecifc pairs of flycatchers had an intermediate response to the seasonal decline in food availability as compared to the two conspecific pairs, and this difference was most pronounced late in the season. To investigate potential mechanisms contributing to this pattern we cross-fostered aviary bred nestling hybrids into nests of pied and collared flycatchers. We were thereby able to compare begging intensity and growth of hybrids with purebred nestlings sharing the same environment. As expected, nestling collared flycatchers begged significantly faster than hybrids, and hybrids had a non-significant tendency to beg faster than pied flycatchers (Fig. 6). By contrast, hybrid nestlings were sig-

17 nificantly heavier than nestling pied flycatchers, but we found no significant differences in weight between nestling collared flycatchers and hybrids. A potential explanation to the observed pattern might be that pied flycatchers breed in a more stable environment late in the season (Veen et al. 2010). In the collared flycatcher nests both hybrids and nestling collared flycatchers increased their begging frequency late in the season whereas such trends were not observed in pied flycatcher nests. In line with our expectations, nestling collared flycatchers also had a lower survival chance compared to nestling hybrids in shared nests.

3.3 3.1 P = 0.02 2.9 2.7 2.5 2.3 2.1 1.9 1.7

Relative meanRelative begging rank 1.50 CF - HY PF - HY

Figure 6. Comparison of relative begging intensity of nestling collared (CF), hybrid (HY) and pied (PF) flycatchers from a cross-fostering experiment in paper III. Hybr- id nestlings were matched against purebred nestlings of the two species in artificially created mixed broods. The graph presents predicted values and s.e. from a mixed effects model (lowest score begs the most). Comparisons were only made between hybrids and pied flycatchers or hybrids and collared flycatchers sharing nests. Sig- nificant differences between the nestlings are indicated by the P-value given above respective bars.

The apparently intermediate life-history adaptations of nestling hybrids mean that they have a fitness disadvantage in the typical environment of the parental species, and selection in terms of nestling fitness is likely to represent an important source of post-zygotic isolation as it acts early in the life cycle. In summary, allopatric divergence can cause environmentally dependent relative fitness of hybrid offspring, and this is also likely to influence the level and direction of gene-flow between the species. Furthermore, adaptations during historic allopatry can be further enhanced during secondary contact, as discussed in paper IV.

18 3.4. The interplay between ecological and reproductive character displacement

When closely related species experience secondary contact they may compete over the same resources (Hardin 1960) and/or interact during mating (“reproductive interference”, reviewed by Gröning and Hochkirch 2008). Harmful interspecific interactions can be reduced through character displacement, i.e. by divergence in resource use or in reproductive phenotypes (Brown and Wilson 1956). Character displacement can result in a pattern of geographical variation where populations in sympatry with a closely related heterospecific differ from conspecific populations in allopatry (Butlin 1987, Howard 1993, Sætre et al. 1997, Noor 1999, Pfennig and Pfennig 2009). As mentioned in section 2, the plumage of male pied flycatchers varies from black and white to brown and white (see cover and paper IV). The brown coloration is more frequent in sympatry with collared flycatchers (Drost 1936, Roskaft and Järvi 1992, Sætre et al 1993, Huhta et al. 1997, Alatalo et al. 1994). This reproductive character displacement in the sexually selected plumage trait between pied and collared flycatchers (Sætre et al. 1997) is often cited as one of the most convincing examples of reinforcement, i.e. the evolution of stronger sexual isolation at secondary contact in response to natural selection against maladaptive hybridization (Dobzhansky 1940).

In paper IV, we investigated the mechanisms behind divergence in three key traits between pied and collared flycatchers breeding on Öland – habitat choice, onset of breeding and plumage coloration. As pied flycatchers breed in woodlots both where collared flycatchers occur and where collared flycatchers are still absent on Öland, this hybrid zone provides a unique opportunity to disentangle the causes and consequences of both ecological and reproductive character displacement. The proportion of deciduous forest in the territories defended by pied flycatchers declined significantly across the study period (Fig. 7), and was ac- companied by a divergence in the onset of breeding between the two flycatcher species. Whereas collared flycatchers advanced their onset of breeding significantly, pied flycatchers did not. This most likely reflects a combination of a plastic response of collared flycatchers to keep up with an advancing peak in food abundance due to recent climate change (Przybylo et al. 2000, Sheldon et al. 2003), and the fact that pied flycatchers are pre- vented from breeding in their preferred habitat and instead being forced out into a new habitat with a later food peak (Veen et al. 2010).

1.00 350 2 0.95 300 11 0.90 250 0.85 16 200 0.80 30 27 150 0.75 19 100 0.70 25 36 0.65 50 PF habitats

Proportion of deciduous trees deciduous of Proportion 0.60 0 Nr. of CF ----- Nr. of breeding collared flycatchers collared breeding of Nr. 2002 2003 2004 2005 2006 2007 2008 2009

Year

Figure 7. The relative proportion of deciduous trees in pied flycatcher territories on Öland has declined across the study period as the number of breeding collared flycatchers (secondary y-axis) has increased. The number of sampled pied flycatcher habitats/year is given below the points.

We did not find any significant further change in the plumage coloration of male pied flycatchers across the study period, probably because plumage coloration is largely a genetically determined trait (Alatalo et al. 1994). However, in contrast to the main expectation of reinforcement, we found that relatively brown male pied flycatchers hybridized more often than black males under similar conditions. In addition, the relationship between male coloration and relative fitness (in terms of reproductive success) among conspecific pairs of pied flycatchers changed depending on the presence or ab- sence of collared flycatchers breeding within the same woodlot. Browner male pied flycatchers experienced higher relative fitness when collared flycatchers were present, whereas the opposite was true in nearby woodlots lacking collared flycatchers (Fig. 8).

20 1.8

1.5

1.2

0.9

0.6

Relative fitness CF absent 0.3 CF present ----- 0 -2-10123 Brown-score of male pied flycatcher

Figure 8. Relative fitness in relation to coloration of male pied flycatchers within the island of Öland. Browner males have relatively higher breeding success than black males in woodlots where collared flycatchers are present (dashed trendline), but relatively lower breeding success in woodlots where collared flycatchers are absent (solid trendline).

We also found that relatively brown male pied flycatchers defended territories that were most dissimilar in habitat composition from the ones defended by collared flycatchers, and that the brownness of male pied flycatchers in areas of co-occurrence with collared flycatchers was significantly related to the habitat composition of the defended territory. Hence, male pied flycatchers with the most divergent strategy compared to collared flycatchers were favored by selection. In paper IV we argue that reproductive character displacement, observed in the plumage and the timing of breeding, and ecological character displacement in terms of a shift in habitat occupancy, of male pied flycatchers co-occurring with collared flycatchers is initially driven by intense social and ecological interactions with a dominant competitor rather than by avoid- ance of hybridization (i.e. reinforcement). Our results further imply a feedback loop between ecological divergence and reproductive character displacement, which may have important consequences during the final stages of the speciation process.

3.5. The role of early learning in causing shifts in habitat choice A recurrent theme of my thesis has been that increasing numbers of collared flycatchers has severe implications for pied flycatchers, e.g. for population dynamics (paper I, II), hybridization risk (paper I, III), relative fitness (paper IV), breeding time (paper IV) and habitat choice (paper IV). To escape in-

21 terspecific competition pied flycatchers have been forced out towards a less preferred, lower quality habitat (paper IV). Again, this raises the question of competitive exclusion (see introduction). If pied flycatchers have a genetic preference for the same hazel/oak forests as collared flycatchers prefer to breed in, recruitment would still proceed into these areas, with a risk of un- successful establishment, which in a longer perspective could increase the risk of a regional extinction. Many models on the evolution of habitat isolation assume that habitat choice is a genetically determined trait (see Beltman and Metz 2005 and references therein), although learned habitat choice is known to occur in several animal species (Davis and Stamps 2004). In paper V we show that the observed habitat divergence between pied and collared flycatchers increases pre-mating isolation, and we investigated how an enforced habitat shift can be maintained. By cross-fostering eggs and nestlings between pied and collared flycatcher nests we were able to show that the recruits, i.e. one year old birds returning to breed, subsequently settled to breed significantly closer to their foster parents’ nest than to their genetic parents’ nest (Fig. 9). The habitat composition of the pied and collared flycatcher territories in this study were found to be significantly different (with a higher proportion of coniferous trees in pied flycatcher territories), i.e. the recruits settled closer to their foster parents even though they had been translocated between different types of habitats. In paper V we argue that learned habitat choice can play an important role in enhancing reproductive isolation and facilitate regional coexistence at secondary contact between diverging populations.

Nest of genetic parents Nest of foster parents

Mean distance = Mean distance = 22754 m 1022 m

Own breeding nest consecutive year

Figure 9. Yearling birds recruited from the cross-fostering experiment between pied and collared flycatchers in paper V subsequently settled to breed significantly closer to their foster parents than to their genetic parents, even when translocated across different habitats.

22 4. Conclusions and future perspectives

4.1. Competition and coexistence

In this thesis, I have shown that pied flycatchers are being rapidly excluded by collared flycatchers from the most favorable breeding sites on Öland (papers I, II). Young male pied flycatchers are having increasing difficulties in establishing territories in areas shared with collared flycatchers, with increasing rates of heterospecific pairing among female pied flycatchers as a side-effect (paper I). Hence, there is a feedback effect such that competitive exclusion is affecting the rate of hybridization, which is likely to speed up the exclusion of pied flycatchers as hybridization is associated with a high fitness cost. The interactions between competition and hybridization have been largely overlooked in evolutionary ecology. My findings show that it is important to consider age- and sex biased effects of competition, which in turn can affect the risk of hybridization (paper I). Global change is supposed to increase the prevalence of biological invaders (Dukes and Mooney 1999) and previously separated species are being brought together at an increasing speed (Parme- san and Yohe 2003). Still, it remains largely untested how interactions between different elements of global change might affect interactions between closely related species. The relative effects of interspecific competition and hybridization could vary in relation to biotic as well as abiotic factors, which is an area that requires further research. Divergence in life-history traits initiated during historic allopatry can facilitate habitat divergence and coexistence at secondary contact (paper II, IV). Hence, my findings provide support both for models on species coexistence that emphasize the importance of spatial or temporal heterogeneity in causing changes in relative fitness (e.g. Chesson and Huntley 1997, Amarasekare and Nisbet 2001), and for studies emphasizing the importance of life-history trade-offs (e.g., Bonsall et al. 2004). The mechanisms of coexistence seem to be rather similar for sexually interacting species (e.g. Gröning and Hoch- kirch 2008), which is relevant in the flycatcher case since hybridization is, as mentioned above, likely to speed up local extinction once one of the two species has become rare. The rapid divergence in breeding habitat between the two flycatcher species (paper IV) implies that habitat heterogeneity per se may be an important

23 target for conservation. However, increasing habitat segregation may also have negative effects on population dynamics from a long-term perspective. We show that competition over limited breeding habitat can result in asymmetric niche segregation, so that only the competitively inferior species is forced to utilize the lower-quality habitats. Lower food availability and/or quality may support a smaller population of the competitively inferior species than would be possible in the high-quality habitat, and small populations risk extinction due to stochastic demographic or environmental effects. Once hybridization and interference competition lead to local extinction of the inferior species, because of the asymmetric niche segregation, these forces may continue to indirectly influence the population dynamics of this species and enhance the likelihood of a more regional extinction. These types of questions beg for theoretical modelling, incorporating the relative effects of competition and hybridization in relation to environmental conditions.

4.3. Evolutionary implications

How can rapid habitat divergence be maintained and increase reproductive isolation? If habitat choice is a genetically determined trait (which is often assumed in models on sympatric speciation), recruitment would still proceed into the preferred habitat, with a risk of competitive and/or sexual exclusion. When one species shifts breeding habitat due to interspecific competition and/or hybridization, segregation in habitat choice will increase (leading to enhanced premating isolation as a side effect) when recruitment into the alternative environment exceeds recruitment into the originally preferred environment due to learning (i.e. imprinting on the natal environment). Thus, learned habitat choice may play an important role both in enhancing reproductive isolation and in facilitating regional coexistence at secondary contact between diverging populations (paper V). Divergence in reproductive phenotypes, more specifically plumage coloration, between pied and collared flycatchers has become a text-book example of reinforcement, i.e. the evolution of stronger sexual isolation at secondary contact between populations as a response to natural selection against maladaptive hybridization (Dobzhansky 1940), where male pied flycatchers occurring in sympatry with collared flycatchers are browner compared to allopatric populations of pied flycatchers (Drost 1936, Roskaft and Järvi 1992, Sætre et al. 1993, Huhta et al. 1997). However, in paper IV we found that on Öland, relatively brown male pied flycatchers experienced higher fitness than black male pied flycatchers in areas shared with collared flycatchers, whereas the opposite was true in areas where collared flycatchers were absent. These results were consistent with earlier findings that interspecific aggression is relaxed for brown male pied flycatchers (Král et al. 1988, Gustafsson and Pärt 1991, Sætre et al. 1993). We also found that browner

24 male pied flycatchers were more likely to hybridize as compared to black male pied flycatchers, i.e. the ability to coexist with collared flycatchers comes with an increased risk of hybridizing. Our results hence suggest that the role of reinforcement in the speciation of Ficedula flycatchers based on the geographical pattern of plumage variation has been overestimated, while the role of competition between males has been underestimated, especially in the initial stages in the process of reproductive character displacement. We also show that reproductive traits (plumage coloration in this case) can influence which territory a male can obtain, and we found that the males with the most divergent strategy compared to the dominant competitor were favored by selection. We therefore suggest that a feedback loop between ecological divergence and reproductive character displacement through male interspecific competition may play an important role during the final stages of speciation. Different adaptations during historic allopatry are important in facilitating coexistence, but also in providing a foundation for further divergence at secondary contact (Fig. 10). This mechanism by which the speciation process could be finalized in sympatry could moreover act during a much wider range of conditions than reinforcement: selection for avoiding interspecific male competition can remain high even when the rate of hybridization is low.

Competition Hybridization

Local extinction Character displacement: -habitat -timing of breeding -plumage Regional coexistence

Environmental heterogeneity and life-history trade-offs

Figure 10. A summary of the complex ecological and evolutionary interactions studied in this thesis. Positive relationships are indicated by solid arrows, and negative relationships with dashed arrows.

25 5. Sammanfattning på svenska

Samexistens mellan närbesläktade arter har länge fascinerat forskarsamhäl- let. Vilka mekanismer möjliggör samexistens? Hur viktiga är mellanarts interaktioner som konkurrens och hybridisering för utdöenden respektive artbildning? Frågeställningar som dessa är mer relevanta idag än någonsin när bl.a. habitatstörningar och klimatförändringar gör att arters utbredningar snabbt förändras. Detta innebär bl.a. att tidigare åtskiljda närbesläktade arter exponeras för varandra i en ökande takt. I den här avhandlingen har jag undersökt ekologiska och evolutionära ef- fekter av konkurrens, hybridisering och divergens i livshistoriekaraktärer (karaktärer förknippade med överlevnad och reproduktion) mellan två när- stående arter av flugsnappare; svartvit- (Ficedula hypoleuca) och halsbandsflugsnappare (F. albicollis). I Sverige häckar båda arterna på Öland och Got- land. Artiklarna i avhandlingen baseras på empiriska och experimentella data insamlade på Öland.

Studiesystem

Man uppskattar att halsbandsflugsnapparen dök upp på Gotland för ca. 150 år sedan, och på Öland så sent som i slutet på 50-talet/början på 60-talet. Halsbandsflugsnapparen är något större samt har mer markerade ornament jämfört med hannen hos svartvit flugsnappare. Utöver ett vitt halsband, som namnet antyder, så har halsbandshannen en stor vit pannfläck och mycket vitt på vingarna (Fig. 2). Fjäderdräkten hos den svartvita hannen varierar mellan just svart och vitt till mera honlikt brunt och vitt (se omslag och artikel IV). Den brunvita dräkten är vanligare när den svartvita flugsnapparen samexisterar med halsbandsflugsnappare, ett fenomen som kallas ”character displacement” (karaktärsförskjutning), och antas vara en evolutionär respons för att undvika hybridisering. Fjäderdräkten utgör en s.k. reproduktiv barriär, och en förskjutning i områden av samexistens (sympatri) refereras till som ”reinforcement” (förstärkning) i artbildningssammanhang. Sången är lätt att skilja mellan arterna, men på Öland och Gotland är det är vanligt att svartvita hannar väver in strofer från halsbandflugsnapparen i sin repertoar. Varningslätena är också artspecifika och utgör en bra karaktär för identifikation (gäller även honor). Honorna hos de två arterna är mer lika

26 varandra i utseende. Den svartvita honan är dock något mindre och brunare i färgen än halsbandshonan som har en gråare ton. Den pågående långtidsstudien av flugsnappare på Öland initierades 2001- 2002 och omfattar idag ca. 2000 holkar i 21 olika områden spridda över ön. Ett av områdena övervakades också mellan åren 1981-85.

Mål med avhandlingen

Mina mål med den här avhandlingen har varit att undersöka de ekologiska och evolutionära effekterna av sekundär kontakt mellan två närstående arter. Hur viktiga är skillnader i livshistoriekaraktärer som ackumulerats mellan arterna när de varit åtskiljda för att underlätta samexistens och för att ytterligare förstärka reproduktiva barriärer vid sekundär kontakt? Hur påverkar mellanarts interaktioner val av habitat och häckningstid? Mer specifikt så har jag undersökt: de relativa effekterna av konkurrens och hybridisering för lokala utdöenden (artikel I), betydelsen av divergens i livshistoriekaraktärer för samexistens (artikel II), betydelsen av divergens i livshistoriekaraktärer för hur hybrider mellan arterna presterar i olika miljöer (artikel III), sambandet mellan ekologiska och reproduktiva karaktärsför- skjutningar (artikel IV), och betydelsen av tidig inlärning för valet av häck- ningshabitat (artikel V).

Sammanfattning av huvudsakliga resultat

Halsbandsflugsnapparen började kolonisera Öland runt staden Löttorp på norra delen av ön. I artkel I visar jag att halsbandsflugsnapparen nu håller på att driva den svartvita flugsnapparen mot utrotningens rand i det här områ- det. Mellan åren 2002-2009 var det en signifikant nergång i antalet svartvita flugsnappare till fördel för halsbandsflugsnapparen i det här området, där- emot minskade inte antalet svartvita flugsnappare på fastlandet eller i områ- den på Öland utan halsbandsflugsnappare under samma tidsperiod. Vi fann inga skillnader mellan arterna när vi jämförde ankomstdatum, kullstorlek, häckningsframgång och livslängd hos hannarna, dvs de hannar hos svartvita flugsnapparen som lyckades etablera sig klarade sig lika bra som halsbands- flugnapparna, en indikation på att konkurrens om mat inte är den huvudsakliga orsaken till minskningen av svartvita flugsnappare. Däremot häckade halsbandsflugsnapparen tidigare än den svartvita flugsnapparen, och medan hanliga nyetableringar (d.v.s. unga hannar som häckar för första gången) av halsbandsflugsnappare ökade över tid, så minskade nyetableringen av svartvita hannar. Med andra ord så har unga svartvita hannar ökande problem med att få tillgång till holkarna. Ett liknande mönster observerades hos de svartvita honorna, men något förskjutet i förhållande till hannarna. En kon-

27 sekvens av detta var en ökande frekvens av hybridisering mellan svartvita honor och halsbandshannar över tid, vilket ytterligare skyndar på exklude- ringen av svartvita flugsnappare (honliga hybrider är sterila och hanliga hybrider har reducerad fertilitet samt svårt att hitta partners).

I artikel II undersökte jag vilka faktorer som underlättar samexistens mellan dessa två närbesläktade och konkurrerande arter. Genom ett experiment där vi partiellt delade på kullar och därefter flyttade ungarna mellan arternas bon kunde vi jämföra tillväxt och mortalitet mellan arterna över häckningssä- songen. För att simulera ”bra” förhållanden minskade vi vissa bon med två ungar, respektive utökade vissa bon med två ungar för att simulera ”tuffa” förhållanden. Halsbandsflugsnapparens ungar har tidigare visat sig vara mer aggressiva i sitt tiggningsbeteende jämfört med svartvita ungar. Våra resultat i artikel II visar att halsbandsflugsnapparens ungar också var känsligare än svartvita flugsnapparens ungar för den minskande tillgången på mat sent på säsongen. Halsbandsflugsnapparens ungar var signifikant tyngre än ungarna från svartvita flugsnappare vid tre dagars ålder. Det var dock en negativ kor- relation mellan vikt ökningen från dag tre till dag tolv och häckningstidpunk- ten hos halsbandsflugsnapparens ungar i bon där kullstorleken utökats, men inte i bon där kullstorleken reducerats. Detta antyder att den generellt något mindre kullstorleken hos halsbandsflugsnappare jämfört med svartvita flugsnappare utgör en adaptiv anpassning till halsbandsflugsnapparens ungars högre känslighet för låg tillgång på föda. De här skillnaderna i livshistorieka- raktärer har grundats i perioder när arterna varit åtskiljda (allopatriska), den svartvita flugsnapparen har funnits längre på nordliga breddgrader och är därför bättre anpassad till de relativt varierande klimat och habitat betingelserna. I artikel II argumenterar vi att denna miljörelaterade skillnad i ungar- nas känslighet underlättar samexistens mellan arterna, och avgör när den mer aggressiva halsbandsflugsnapparen kan konkurrera ut den svartvita flugsnapparen.

Artikel III fortsätter på temat livshistoriekaraktärer, men med fokus på hybrider mellan de två föräldraarterna. Livshistoriekaraktärer är viktiga vid lokala anpassningar till t.ex. variationer i klimat, framförallt i stadium när arterna har svårt att undkomma att exponeras för miljön, t.ex. i det juvenila stadiet. Det finns också indikationer på att divergens i livshistoriekaraktärer kan vara kopplat till reproduktiv isolering. Genom att para halsbandshonor med svartvita hannar i ett burexperiment, kunde vi placera ut hybrid av- komman i naturliga bon av halsbands- och svartvita flugsnappare för att jämföra deras prestationer i form av tiggningsbeteende och tillväxt. Ungar av halsbandsflugsnappare tiggde signifikant snabbare än hybrider i samma bon, men det var ingen skillnad i vikt mellan de två typerna av ungar. I bon för- svarade av svartvita flugsnappare så var hybriderna signifikant tyngre än ungarna av svartvita flugsnappare, men det var ingen signifikant skillnad i

28 tiggningsbeteende (hybrider tenderade dock att tigga snabbare). En potentiell förklaring till dessa resultat kan vara att svartvita flugsnappare häckar i en mer stabil miljö sent på säsongen och/eller är bättre på att lokalisera föda. Experimenten utfördes relativt sent på säsongen när häckningsframgången skiljer sig mellan arterna; svartvita flugsnappare klarar sig bättre än halsbandsflugsnappare sent på säsongen, och blandpar har en intermediär häck- ningsframgång. Våra resultat bidrar med en partiell förklaring till det här mönstret. De genetiska skillnaderna mellan hybrider och de ”rena” arterna gör att miljöbetingelserna påverkar hur hybriderna klarar sig, och därmed också riktningen och nivån på genflödet mellan arterna. Allopatrisk divergens i livshistoriekaraktärer kan därför spela en viktig roll för den reproduktiva isoleringen mellan arter vid sekundär kontakt, och också utgöra en grund för vidare divergens, vilket vi studerade i artikel IV.

Som tidigare nämnts så varierar fjäderdräkten hos den svartvita flugsnappar- hannen från svart och vit till brun och vit, och den bruna varianten är vanligare i områden där de samexisterar med halsbandsflugsnappare. Detta fenomen utgör ett exempel på reproduktiv karaktärsförskjutning och antas bero på en artbildningsprocess som kallas reinforcement (förstärkning). Reinfor- cement kan sägas vara naturlig selektion mot hybridisering. I artikel IV undersökte vi orsakerna bakom förskjutningar i tre viktiga ka- raktärer mellan svartvit och halsbandsflugsnappare: förutom fjäderdräkt också val av häckningshabitat och häckningstidpunkt. På Öland häckar den svartvita flugsnapparen både i områden tillsammans med halsbandsflugsnapparen (högproduktiv ädellövskog), och i områden utan halsbandsflugsnappare (lågproduktiv barrdominerad skog). Vi fann att bruna hannar hos den svartvita flugsnapparen hade högre häckningsframgång än svarta hannar i områden med halsbandsflugsnappare, men lägre häckningsfram- gång i områden utan halsbandsflugsnappare. Till vår förvåning fann vi också att relativt bruna hannar också var mer benägna att hybridisera. Dessa upp- täckter antyder att det inte finns någon honlig preferens för bruna hannar på Öland, och att undvikande av hybridisering inte är den primära orsaken till denna karaktärsförskjutning, åtminstone inte i detta stadium av samexistens. Bruna hannar hos svartvita flugsnappare har tidigare visat sig undkomma aggressiva interaktioner från halsbandsflugsnappare, och har därför en bättre chans att samexistera med dem. Detta leder dock till en ökad risk för hybridisering. Vi fann också att andelen lövskog i svartvita habitat minskade över tid (ekologisk karaktärsförskjutning), och att denna förskjutning ackompan- jerades av en allt senare häckningstid (reproduktiv karaktärsförskjutning). Detta beror antagligen dels på att den aggressivare halsbandsflugsnapparen förhindrar den svartvita flugsnapparen från att häcka tidigt, men också på att födotillgången är som högst något senare i barrskog jämfört med lövskog. Brunheten i fjäderdräkten påverkade vilket habitat de svartvita hannarna fick tillgång till, och vi fann att de svartvita hannarna med den mest diverge-

29 rade strategin jämfört med halsbandshannar gynnades av selektion. Våra resultat visar på en återkoppling mellan ekologisk divergens och reproduktiv karaktärsförskjutning som förmodligen spelar en viktig roll för att förstärka den reproduktiva isoleringen mellan närbesläktade arter.

I den här avhandlingen har jag beskrivit ganska dramatiska konsekvenser för svartvita flugsnappare på Öland som en direkt följd av ett snabbt ökande antal halsbandsflugsnappare. Betyder det här att svartvita flugsnappare kommer att exkluderas från Öland inom en snar framtid? Om svartvita flugsnappare har en genetisk preferens för samma habitat som halsbandsflugsnappare så kommer rekryterna (fåglar som föds i området och sedan återvänder för att häcka) att fortsätta försöka etablera sig i de lövskogsrika områdena, med en stor risk att misslyckas. Om preferensen för häckningsha- bitatet däremot är inlärd så kommer det att förstärka förskjutningen mot ett mer barrdominerat häckningshabitat. Jag flyttade hela kullar av ägg mellan arternas bon för att undersöka om rekryterna etablerade sig närmre sitt ur- sprungliga” genetiska” bo, eller sitt nya ”foster” bo. Jag använde mig även av rekryter från omförflyttnings experiment utförda tidigare år. Det var en signifikant skillnad i habitat struktur mellan föräldraarterna, med ett större inslag av barrskog i svartvita habitat. Trots detta fann vi att rekryterna etablerade sig signifikant närmre sina fosterföräldrar än sina genetiska föräld- rar. Vi hävdar i artikel V att inlärda habitatpreferenser därmed också är viktiga för att underlätta samexistens och ytterligare förstärka den reproduktiva isoleringen mellan arterna, något som tidigare varit ganska förbisett i forskning kring artbildning.

30 6. Acknowledgements

First of all, I would like to thank Anna for giving me this opportunity. It’s been a bumpy ride at times, but you’ve always been there to support me. Discussing ideas with you is inspiring, and you always seem to have a card up your sleeve. You also have a very sound and humble attitude towards science (and life in general), making it easy to go to work. Many thanks also to my second supervisor Lars, a.k.a. the flycatcher-guru, for taking me on as a student and for sharing your knowledge. Thanks to Mats for giving me a desk to sit by, and for showing me Helsinki by night. I would also like to thank Anders Ö and Olle H for bringing me here in the first place, and for making me realize how fun science can be!

It’s been a privilege to be a part of Anna’s dynamic group for a few intensive years, and I hope our paths will cross again in one way or the other. Andreas, thanks for good laughs and perspectives beyond birds. Hanna, thanks for helping to sort out the first confusing experiences of grad school and field work. Kasia, thanks for an inspiring devotion to science. Horses trampling your SAAB, flat tires, ticks and fleas, rainstorms, trolls in the lab - nothing can stop you. Keep it up! Amber, thanks for always being positive and will- ing to help, no matter what the circumstances. You also brought some fancy American cuisine (e.g. peanutbutter/banana sandwiches) and musical arts (e.g. snuff sniffin’ woman) that improved the quality of the field seasons significantly. Arild, thanks for patiently putting up with my questions about all sorts of statistical issues, for commenting on drafts, and for strongly pro- moting the Norwegian cultural heritage (i.e. Ole-Ivars). Mårten, thanks for bringing both birds and beers to Öland. Richard and Matt, thanks for sharing some of your Anglo-Saxon wisdom. Murielle, thanks for “taking over” (and for a good taste in music).

I would like to thank all the field assistants and students who helped collect- ing data over the years: Markus, Helene W, Sofia, Beata, Erik, Emelie, Eli- sabeth, Fredrik, Friedrike, Stina, Matthieu, Hanna O., Helene O, Vendela, Lisa, Anders, Johnny. You did an amazing job (and some of you even came back for another year!). A special thanks to Jue and Yuki who put down a lot of work both in the field and in analyzing recordings. Thanks to Nisse Pers- son for providing nest-boxes and aviaries. Thanks to my predecessors Chris and Nina who taught me how to find invisible nest-boxes and all that. The

31 fact that both of you ended up in Australia bothers me a bit though. Thanks Yvonne and Bosse for being the best landlords one could ask for. The friend- ly atmosphere at your place helped a lot when being homesick.

Teaching and meeting students has been a great experience during this time. I would like to thank Anders Ö, Hanna, Johanna and Jenny for exploring some good (and some not so good?) pedagogical ideas with me. Thanks also to Ingrid for valuable advice and support, and to Anders B for assigning me interesting classes. Thanks to Hwei-Yen and Felix for nice company in the office. The same goes for Emma and Marnie despite the morning routine... Thanks to Göran A, Reija and Ingela for help with various complicated stuff. Thanks to Elena and Amber for correcting my English here and there. Many thanks of course to all past and present inhabitants of the Animal Ecology corridor and EBC during these years; it’s been a nice place to be. I would also like to acknowledge Stiftelsen för Zoologisk Forskning, Kungliga Ve- tenskaps-Akademien,Värmlands Nation, Sveriges Ornitologiska Förening, EBC graduate school on Genomes and Phenotypes and Rektors resebidrag från Wallenbergstiftelsen for awarding me grants which enabled me to par- ticipate at conferences and purchase equipment and literature during my PhD. Thanks to Johan Träff and Måns Hjernquist for stunning pictures and artwork.

Kerstin and Göran, many thanks for looking after my family/house/ gar- den/pets/car when I’ve been away. I couldn’t have done it without you! Thanks also to Staffan and Marie, Marco and Anna, and Henrik and Linda with families for helping out and being good friends and neighbours. We miss you Linda. Thanks to Lars E, Hans B.A and Hans-E for letting my mind off science every now and then. Thanks to my sisters Helené, Teresia and Jenny with families for nice company/travels/weddings (and thanks for the relascope, skogs-Micke). Thanks to mom and dad, Britt-Marie and Seved, for supporting me on the crooked road that is my life, even though my interest in nature manifested itself in this way rather than in a fish- ing/hunting kind of way ;^)

Most of all, I would like to thank my beautiful girls back home, Carina, Alva and Thea, for your patience and support. Being away from you so much has been the hardest part about this thesis. You are amazing and I love you, always.

32 7. References

Alatalo, R. V., Gustafsson, L. & Lundberg, A. (1994) Male coloration and species recognition in sympatric flycatchers. Proceedings of the Royal Society of London Series B-Biological Sciences, 256: 113-118. Amarasekare, P. & Nisbet, R. M. (2001) Spatial heterogeneity, source-sink dynamics, and the local coexistence of competing species. American Naturalist, 158: 572-584. Anderson, C. N. & Grether, G. F. (2010) Interspecific aggression and character displacement of competitor recognition in Hetaerina damselflies. Proceedings of the Royal Society B-Biological Sciences, 277: 549-555. Arnold, M. L. (1997) Natural hybridization and evolution. Oxford Universi- ty Press, New York. Barton, N. H. & Hewitt, G. M. (1985) Analysis of hybrid zones. Annual Review of Ecology and Systematics, 16: 113-148. Beltman, J. B. & Metz, J. A. J. (2005) Speciation: more likely through a genetic or through a learned habitat preference? Proceedings of the Royal Society B-Biological Sciences, 272: 1455-1463. Blair, W. F. (1974) Character displacement in frogs. American Zoologist, 14: 1119-1125. Bonsall, M. B., Jansen, V. A. A. & Hassell, M. P. (2004) Life history trade- offs assemble ecological guilds. Science, 306: 111-114. Brown, W. L. & Wilson, E. O. (1956) Character Displacement. Systematic Zoology, 5: 49-64. Butcher, G. S. & Rohwer, S. (1989) The evolution of conspicuous and dis- tinctive coloration for communication in birds. Current Ornithology, 6: 51-108. Butlin, R. (1987) Speciation by reinforcement. Trends in Ecology & Evolu- tion, 2: 8-13. Chesson, P. & Huntly, N. (1997) The roles of harsh and fluctuating conditions in the dynamics of ecological communities. American Naturalist, 150: 519-553. Confer, J. L. (2006) Secondary contact and introgression of Golden-winged warblers (Vermivora chrysoptera): documenting the mechanism. The Auk, 123: 958-961. Coyne, J. A. & Orr, H. A. (2004) Speciation, Sunderland, Massachusetts, Sinauer Associates, Inc. Darwin, C. (1859) On the origin of species by means of natural selection, London, John Murray. Davis, J. M. & Stamps, J. A. (2004) The effect of natal experience on habitat preferences. Trends in Ecology & Evolution, 19: 411-416.

33 Dobzhansky, T. (1937) Genetics and the Origin of Species. Columbia Uni- versity Press, New York. Dobzhansky, T. (1940) Speciation as a stage in evolutionary divergence. American Naturalist, 74: 312-321. Drost, R. (1936) Über das Brutkleid männlicher Trauerfliegenfänger, Musci- capa hypoleuca. Vogelzug, 6:179-186. Dukes, J. S. & Mooney, H. A. (1999) Does global change increase the success of biological invaders? Trends in Ecology & Evolution, 14: 135-139. Feder, J. L., Opp, S. B., Wlazlo, B., Reynolds, K., Go, W. & Spisak, S. (1994) Host fidelity is an effective premating barrier between sympatric races of the apple maggot fly. Proceedings of the National Academy of Sciences of the United States of America, 91: 7990-7994. Gause, G. F. (1934) The struggle for existence. NewYork: Hafner. Grant, B. R. & Grant, P. R. (1993) Evolution of Darwin finches caused by a rare climatic event. Proceedings of the Royal Society of London Series B- Biological Sciences, 252: 253-253. Grether, G. F., Losin, N., Anderson, C. N. & Okamoto, K. (2009) The role of interspecific interference competition in character displacement and the evolution of competitor recognition. Biological Reviews, 84: 617-635. Gröning, J. & Hochkirch, A. (2008) Reproductive interference between animal species. Quarterly Review of Biology, 83: 257-282. Gustafsson, L. & Pärt, T. (1991) Interspecific relations between collared and pied flycatchers. Proceedings from the XX International Ornithologist Congress, 20:1425-1431. Hardin, G. (1960) Competitive Exclusion Principle. Science, 131: 1292- 1297. Haskell, D. (1994) Experimental evidence that nestling begging behavior incurs a cost due to nest predation. Proceedings of the Royal Society of London Series B-Biological Sciences, 257: 161-164. Hatfield, T. & Schluter, D. (1999) Ecological speciation in sticklebacks: Environment-dependent hybrid fitness. Evolution, 53: 866-873. Hendry, A. P. & Day, T. (2005) Population structure attributable to reproductive time: isolation by time and adaptation by time. Molecular Ecol- ogy, 14: 901-916. Helbig, A. J. (1991) Inheritance of migratory direction in a bird species - a cross-breeding experiment with Se-migrating and Sw-migrating Black- caps (Sylvia atricapilla). Behavioral Ecology and Sociobiology, 28: 9-12. Howard, D. J. 1993. Reinforcement: Origin, dynamics, and fate of an evolutionary hypothesis. In Hybrid zones and the evolutionary process (ed. R. G. Harrison), pp 46-69. Oxford University Press, New York, New York, USA. Huhta, E. & Siikamäki, P. (1997) Small scale geographical variation in plumage colour of Pied Flycatcher males. Journal of Avian Biology, 28: 92-94. Jensen, L. F., Hansen, M. M., Pertoldi, C., Holdensgaard, G., Mensberg, K. L. D. & Loeschcke, V. (2008) Local adaptation in brown trout early life-

34 history traits: implications for climate change adaptability. Proceedings of the Royal Society B-Biological Sciences, 275: 2859-2868. Konishi, M. & Takata, K. (2004) Impact of asymmetrical hybridization fol- lowed by sterile F-1 hybrids on species replacement in Pseudorasbora. Conservation Genetics, 5: 463-474. Král, M., Järvi, T. & Bi ík, V. (1988) Interspecific aggression between the collared flycatcher and the pied flycatcher - the selective agent for the evolution of light-colored male pied flycatcher populations. Ornis Scan- dinavica, 19: 287-289. Kuno, E. (1992) Competitive-exclusion through reproductive interference. Researches on Population Ecology, 34: 275-284. Liou, L. W. & Price, T. D. (1994) Speciation by reinforcement of premating isolation. Evolution, 48: 1451-1459. Lewontin, R. C. & Birch, L.C. (1966) Hybridization as a source of variation for adaptation to new environments. Evolution, 20: 315-36. Lotka, A. J. (1932) The growth of mixed populations: two species competing for a common food supply. Journal of the Washington Academy of Sciences, 22: 461-469. Mayr, E. (1942) Systematics and the Origin of Species. Columbia University Press, New York. Moore, J. A. 1957. An embryologist’s view of the species concept. In The species problem (ed. E. Mayr), pp. 325–338. Washington, DC: American Association for the Advancement of Science. Muller, H. J. 1942. Isolating mechanisms, evolution and temperature. Bio- logical Symposium, 6: 71-125. Noor, M. A. F. (1999) Reinforcement and other consequences of sympatry. Heredity, 83: 503-508. Parent, C. E., Caccone, A. & Petren, K. (2008) Colonization and diversification of Galapagos terrestrial fauna: a phylogenetic and biogeographical synthesis. Philosophical Transactions of the Royal Society B-Biological Sciences, 363: 3347-3361. Parmesan, C. & Yohe, G. (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature, 421: 37-42. Pärt, T. & Qvarnström, A. (1997) Badge size in collared flycatchers predicts outcome of male competition over territories. Animal Behaviour, 54: 893- 899. Pfennig, K. S. & Pfennig, D. W. (2009) Character displacement: Ecological and reproductive responses to a common evolutionary problem. Quarter- ly Review of Biology, 84: 253-276. Price, T. D. (2007) Speciation in birds. Greenwood Village, CO: Roberts and Company. Przybylo, R., Sheldon, B. C. & Merila, J. (2000) Climatic effects on breeding and morphology: evidence for phenotypic plasticity. Journal of Ani- mal Ecology, 69: 395-403.

35 Qvarnström, A. (1997) Experimentally increased badge size increases male competition and reduces male parental care in the collared flycatcher. Proceedings of the Royal Society of London Series B-Biological Sciences, 264:1225-1231. Qvarnström, A., Svedin, N., Wiley, C., Veen, T. & Gustafsson, L. (2005) Cross-fostering reveals seasonal changes in the relative fitness of two competing species of flycatchers. Biology Letters, 1: 68-71. Qvarnström, A., Kehlenbeck, J. V., Wiley, C., Svedin, N. & Sæther, S. A. (2007) Species divergence in offspring begging intensity: difference in need or manipulation of parents? Proceedings of the Royal Society B- Biological Sciences, 274: 1003-1008. Rhymer, J. M. & Simberloff, D. (1996) Extinction by hybridization and introgression. Annual Review of Ecology and Systematics, 27: 83-109. Roskaft, E. & Järvi, T. (1992) Interspecific competition and the evolution of plumage-color variation in three closely related old-world flycatchers Fi- cedula spp. Journal of Zoology, 228: 521-532. Rundle, H. D. & Nosil, P. (2005) Ecological speciation. Ecology Letters, 8: 336-352. Sala, O. E. et al. (2000) Biodiversity - Global biodiversity scenarios for the year 2100. Science, 287: 1770-1774. Samietz, J., Salser, M. A. & Dingle, H. (2005) Altitudinal variation in beha- vioural thermoregulation: local adaptation vs. plasticity in California grasshoppers. Journal of Evolutionary Biology, 18: 1087-1096. Sætre, G. P., Kral, M. & Bicik, V. (1993) Experimental evidence for interspecific female mimicry in sympatric Ficedula flycatchers. Evolution, 47: 939-945. Sætre, G. P., Moum, T., Bures, S., Kral, M., Adamjan, M. & Moreno, J. (1997) A sexually selected character displacement in flycatchers rein- forces premating isolation. Nature, 387: 589-592. Schluter, D. (2000) The ecology of adaptive radiation. Oxford University Press, New York, USA. Schluter, D. (2001) Ecology and the origin of species. Trends in Ecology & Evolution, 16: 372-380. Schluter, D. (2009) Evidence for ecological speciation and its alternative. Science, 323: 737-741. Seehausen, O. (2004) Hybridization and adaptive radiation. Trends in Ecol- ogy & Evolution, 19: 198-207. Seehausen, O. & Schluter, D. (2004) Male-male competition and nuptial- colour displacement as a diversifying force in Lake Victoria cichlid fish- es. Proceedings of the Royal Society of London Series B-Biological Sciences, 271: 1345-1353. Servedio, M. R. & Noor, M. A. F. (2003) The role of reinforcement in speciation: Theory and data. Annual Review of Ecology Evolution and Syste- matics, 34: 339-364.

36 Sheldon, B. C., Kruuk, L. E. B. & Merila, J. (2003) Natural selection and inheritance of breeding time and clutch size in the collared flycatcher. Evolution, 57: 406-420. Svensson, L. (1992) Identification guide to European passerines. 4th ed. Märstatryck, Stockholm. Théron, A. & Combes, C. (1995) Asynchrony of infection timing, habitat preference, and sympatric speciation of Schistosome parasites. Evolution, 49: 372-375. Tynkkynen, K., Rantala, M. J. & Suhonen, J. (2004) Interspecific aggression and character displacement in the damselfly Calopteryx splendens. Jour- nal of Evolutionary Biology, 17: 759-767. Tynkkynen, K., Kotiaho, J. S., Luojumaki, M. & Suhonen, J. (2005) Inters- pecific aggression causes negative selection on sexual characters. Evolu- tion, 59: 1838-1843. Veen, T., Sheldon, B. C., Weissing, F. J., Visser, M. E., Qvarnström, A. & Sætre, G. P. (2010) Temporal differences in food abundance promote coexistence between two congeneric passerines. Oecologia, 162: 873- 884. Volterra, V. (1926) Variations and fluctuations of the numbers of individuals in animal species living together. (Reprinted in 1931. In Animal Ecology, ed. R. N. Chapman. New York: McGraw Hill). Wiley, C., Qvarnström, A., Andersson, G., Borge, T. & Sætre, G. P. (2009) Postzygotic isolation over multiple generations of hybrid descendents in a natural hybrid zone: How well do single-generation estimates reflect reproductive isolation? Evolution, 63: 1731-1739. Wolf, D. E., Takebayashi, N. & Rieseberg, L. H. (2001) Predicting the risk of extinction through hybridization. Conservation Biology, 15: 1039- 1053.