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Abstract Relicts are species with a former, more widespread distribution range but can also include specific populations in parts of a species distribution (thus called relict populations). Such populations are often found towards the species range limits where conditions may be less optimal than in the more central parts. For peripheral relict populations to be valuable for conservation from a biodiver-sity point of view, they should be exposed to selection pressures that are different from the more central ones allowing for unique adaptations to arise. I will discuss data from studies of two closely related butterfly species where the aim was to evaluate the uniqueness of marginal relict populations in relation to their more cen-tral counterparts. Neutral genetic variation and values of adaptive wing traits among populations of the scarce heath (Coenonympha hero) and the pearly heath (C. arca-nia) from three biogeographically different regions were compared representing one central and two peripheral parts of their distributions; one peripheral connected to and one isolated from the main area of their distributions. Individuals from the isolated region were significantly differentiated from the peripheral and central regions in both neutral genetic traits and adaptive wing traits, while the peripheral and central populations showed no signs of differentiation in both trait types. I will discuss the possible mechanisms behind the observed patterns and show that the peripheral, relict populations of also widespread species can contribute with valu-able and unique genetic variation. Marginal relict populations constitute ideal study objects of evolution in marginal habitats as they can be used to test how well theory and laboratory experiments reflects more complex natural systems.

1 Introduction

Peripheral populations at the margin of a species’ range may be exposed to ecological and evolutionary processes that differ from more central parts of its distribution. If the level of genetic differentiation is high due to exposure to diversifying

A. Cassel-Lundhagen Department of Ecology, Swedish University of Agricultural Sciences, Ulls väg 16, SE-75007 Uppsala, Sweden e-mail: anna.lundhagen@ekol.slu.se

Peripheral Relict Populations of Widespread Species; Evolutionary Hotspots or Just More of the Same?

Anna Cassel-Lundhagen

J.C. Habel and T. Assmann (eds.), Relict Species: Phylogeography and Conservation Biology,DOI 10.1007/978-3-540-92160-8_15, © Springer-Verlag Berlin Heidelberg 2010

268 A. Cassel-Lundhagen

processes, like random genetic drift and selection, this could eventually lead to speciation (Garcia-Ramos and Kirkpatrick 1997; Mayr 1954, 1963). Thus, such peripheral populations may be unique and important from a conservation point of view (Channell and Lomolino 2000; Lesica and Allendorf 1995).

Relicts are defined as species with a former more widespread distribution range but can also include specific populations in parts of a species distribution (thus called relict populations). Such populations are often found towards the species range limits where conditions may be less optimal than in more central parts (i.e. Gullberg et al. 1998). One could argue that peripheral relict populations of globally widespread species should not be prioritized for conservation as they constitute only a marginal fraction of the species in the global biodiversity. However, both evolutionary history and local selection pressures may differ along a species distri-bution range and this can lead to unique genotypes and adaptations that are not present elsewhere (Eckert et al. 2008). Especially, peripheral populations of species with limited dispersal capacity are likely to originate from populations that have gone through recurrent bottlenecks during colonization and differentiation can then be rapid and significant if founders are few (Chakraborty and Nei 1977). If the newly established populations lack subsequent gene flow from their sources such effects are expected to remain and accentuate in the region. In addition to the influ-ence of history, genetic drift is likely to be more pronounced towards the range periphery due to a greater influence of stochastic processes. Reduced habitat den-sity as well as climatic constraints will cause size fluctuations of local populations that could cause significant influence of genetic drift with changed allele frequen-cies as a consequence.

Random effects due to founder events and population fluctuations will lead to changes in the neutral or nearly neutral traits. However, for peripheral relict popula-tions to be valuable for conservation, they should also be exposed to selection pres-sures that are different from the ones of more central positions (Lesica and Allendorf 1995). If conditions are equal in all parts of a species range or selection pressure is identical, then these populations could differ significantly in neutral markers, while being identical in selected characters. If conditions instead are diverging, selection will favor genotypes that are different from the best adapted ones in the more central regions (Helgadóttir and Snaydon 1986) causing increased global biodiversity.

Diverging selection pressures may be due to a number of factors and can include differences in local or regional climate, species compositions or landscape struc-tures. In the case of landscape structure, for example, selection pressures can act in favor of increased dispersal capacity (Clare and Hughes 2007) as well as against it (Dempster 1991). With increased isolation among patches and a matrix of low qual-ity (lacking for example resting and foraging sites) dispersers may experience increased mortality leading to selection acting against dispersive genotypes (Cody and Overton 1996; den Boer 1990; Heino and Hanski 2001; Schtickzelle et al. 2006). Such altered behavior is likely reflected also in the individuals’ phenotype (Berwaerts et al. 2006, 2002; Davis 1984; Dempster 1991; Fric and Konvička 2002; Merckx and Van Dyck 2006; Thomas et al. 1998). For example, short and broad

269Peripheral Relict Populations of Widespread Species

wings are expected to favor slow, agile flight and appear to be more common among forms that fly in restricted spaces and dense vegetation (Betts and Wootton 1988).

However, if gene flow from central parts to the periphery is substantial, diversi-fying selection pressures may be hidden due to swamping (Garcia-Ramos and Kirkpatrick 1997). This can occur even if the individual dispersal capacity is equal along the whole range due to a larger net inflow of immigrants into a region with smaller population sizes. Such confounding factors will make discrimination between homogenizing gene flow and lack of diversifying selection problematic and a study setup is needed to allow discrimination among these forces. Studies on peripheral populations should, therefore, be performed including those connected to the main area of the species distribution in some regions and isolated from more central parts in others.

2 Examples From Two Heath Butterfly Species

I will discuss data from studies of two closely related butterfly species where the aim was to evaluate the uniqueness of marginal relict populations in relation to more central counterparts. Patterns in neutral genetic markers and values of adap-tive wing traits among populations of the scarce heath species (Coenonympha hero, Linnaeus, 1761) and the pearly heath species(C. arcania, Linnaeus, 1761) from three biogeographically different regions were compared; one central (central Russia for C. hero and central Europe for C. arcania), one peripheral but connected to the main area of distribution (the Baltic states for both species and termed peripheral region in the following text) and one peripheral and iso-lated (Sweden for both species and termed isolated region in the following text) (Fig. 1a,b).

The Scandinavian populations of C. hero are relicts of a former more widespread distribution within the Scandinavian peninsula (Berglind 1990, 2007) and the spe-cies is therefore classified as “near threatened” in the Swedish Red Data Book (Gärdenfors 2005). On a global scale C. hero is widespread, although locally threat-ened, with a distribution ranging from Japan in the East through central Russia to central Europe in the West. The distribution is fragmentary in Western and Northern Europe and the species is considered threatened in most countries (Eliasson 2005; Kudrna 2002; Tolman and Lewington 1998).

C. arcania has a similar distribution as C. hero with peripheral populations in the Baltic states and Scandinavia, with the difference that it is widely distributed in Europe, from the Northern Mediterranean to South-central Scandinavia and central Estonia (Kesküla 1992; Kudrna 2002). In the East, it is found in Turkey, in Southern Russia and central parts of the Ural Mts. and Transcaucasia (Kudrna 2002; Tolman and Lewington 1998). Although the Swedish populations of C. arcania represent no typical relict due to their distribution being more stable in Scandinavia, they can serve as an illustrating example and a replicate within the described study frame.

270 A. Cassel-Lundhagen

In this study design the aim was to evaluate the patterns found not only in the light of the relative geographic locations of the populations, but also on their his-tory inferred from neutral genetic marker. I discuss results obtained from selec-tively neutral traits, i.e. allozymes (Besold et al. 2008; Cassel and Tammaru 2003), and traits under selection represented by traits describing wing morphology (Cassel-Lundhagen et al. 2009). The allozyme data presented here for C. arcania are based on a subset of populations included in Besold et al. (2008) to make the data sets in each region comparable.

3 Gene Flow

Interestingly there were no indications of gradually reduced levels of genetic vari-ability and gradually increased levels of differentiation from the centre via the peripheral to the isolated region. Instead, the populations in the isolated region had considerably lower levels of variation, while populations in the peripheral region did not differ from the more central ones (Table 1, Fig. 2a,b). Further, the populations in the peripheral populations were only marginally differentiated from the central ones, while the populations in the isolated region were markedly differentiated from both the peripheral and central ones (Table 2). This strongly suggests that the observed pattern is due to a combination of the peripheral and isolated populations’ post-glacial colonization histories and their current position. Gene flow among central and peripheral parts appears to be significant enough to maintain a high level of genetic diversity and low differentiation, while lack of gene flow will cause both reductions in variability as well as differentiation. Thus, having a peripheral position per se does not necessarily lead to genetic loss and dfferentiation.

C

C

PPI I

a b500 km

Fig. 1 Distribution range (marked in light grey) of (a) the scarce heath butterfly (Coenonympha hero) and (b) the pearly heath butterfly (Coenonympha arcania) in Europe and western Asia. Dark grey circles indicate sampling sites of both species representing central (C), peripheral (P) and isolated (I) parts of their distributions

271Peripheral Relict Populations of Widespread Species

Table 1 Comparison of allozyme diversity measures for C. hero and C. arcania in a central, a peripheral and an isolated region of the two species distributions. Measures include percentage of polymorphic loci where the frequency of the most common allele does not exceed 0.95 (P

95% loci),

allelic richness, observed heterozygosity (Hobs

) and expected heterozygosity (Hexp

)

C. hero

Regions P95%

loci Allelic richness Hobs

Hexp

Isolated 16.7 1.20 0.03 0.03Peripheral 20.0 1.43 0.09 0.12Central 35.0 1.58 0.09 0.11Differences among regionsa

Isolated/peripheral n.s. n.s. ** *Isolated/central ** ** ** **Peripheral/central n.s n.s. n.s. n.s.

C. arcaniaRegions P

95% loci Allelic richness H

obsH

exp

Isolated 20.4 1.31 0.08 0.09Peripheral 54.6 1.93 0.18 0.21Central 45.8 2.06 0.18 0.20Differences among regionsIsolated/peripheral ** *** *** ***Isolated/central *** *** *** ***Peripheral/central n.s. n.s. n.s. n.s.an.s. = non significant, *p < 0.05, **p < 0.01, ***p < 0.001

4 Selection Vs. Gene Flow

The adaptive traits representing overall wing size and shape followed the same pattern as the neutral markers. Individuals from the isolated region were significantly differentiated from the peripheral and central while the peripheral and central popu-lations showed no signs of differentiation. If predicting that selection pressures are equal in the peripheral and isolated region, low or lacking levels of differentiation in both neutral and selected traits in the peripheral populations in combination with a significant differentiation in both marker types in the isolated populations suggest that gene swamping is causing the observed pattern. This is supported by the fact that the peripheral and isolated regions are found on the same latitude while the central populations are found on an order of magnitude more distant, suggesting that environmental conditions should be more equal in the peripheral regions rather than the peripheral and central ones.

However, I cannot from current data exclude that there are actually different selection pressures in the two peripheral regions. For at least two reasons both species experience a more fragmented landscape in Sweden than in the Baltic states. Firstly, Southern Sweden has a history of great changes in landscape configuration due to an intensive afforestation over the last century (Nilsson 1990), while the

272 A. Cassel-Lundhagen

Table 2 Fixation index (FRT

) and their significances among three regions of the two species C. hero and C. arcania within their distribution range

Regions C. hero C. arcania

Isolated/peripheral 0.26** 0.06***Isolated/central 0.12** 0.04**Peripheral/central 0.07** 0.01**

**p < 0.01, ***p < 0.001See text for definition of regions

Fig. 2 Expected heterozygosity (± S.E.) for (a) 10 allozyme loci plotted against longitudinal position for 13 populations of C. hero and (b) 18 allozyme loci plotted against latidudinal position for 16 populations of C. arcania. Populations originate from three parts of the species’ distribu-tions; one core (Ural for C. hero and central Europe for C. arcania, population means indicated as straight line), one peripheral (Estonia for both, population means indicated as stars) and one iso-lated (Sweden for both, population means indicated as rombs)

273Peripheral Relict Populations of Widespread Species

landscape structure has not changed considerably in, for example, Estonia during the same time period (Palang et al. 1998). Secondly, due to a significant decline in low intensive agriculture in Sweden over the past century (Dahlström et al. 2006), the proportion of semi-natural grasslands (primary habitats of Coenonympha species (Eliasson et al. 2005) is definitely lower in Sweden compared to the Baltic states. Both these processes have lead to lower amounts of available habitat for the Swedish butterflies. As a consequence, both Coenonympha species may occur to a larger extent as locally isolated populations in Sweden, whereas the distribution approaches a continuous one in the peripheral Baltic (states) region.

5 Additional Threats to Peripheral Relict Populations

As described above, peripheral relict populations can also experience reduced levels of genetic variation which may reduce their potential to adapt to the envi-ronment and/or cope with stress (Bulmer 1971; Roff 1997). Therefore, even if peripheral relict populations are genetically unique their peripheral position can also cause an additional constraint to their survival capacity, where isolation may threaten their existence if the loss of variation adversely affects their current performance and ability to cope with changes in living conditions. In addition, if peripheral conditions select for less dispersive phenotypes, as appears to be the case in the examples described here, this will adversely affect their ability to react to improved climatic conditions. Even if a new habitat is created beyond the species current distribution range, the species may have lost their ability to track the newly created habitat if selection has removed good dispersers from the gene pool. If the differences observed are mirrored in flight performance, I could then expect that these peripheral populations can differ in reactivity to climate change (Haynes and Cronin 2006). Thus, individuals of the species found at the same range margin may differ in their reaction to changing climatic conditions and this should be taken into account when predicting the effects of climate change on species communities.

6 Conclusions

Irrespective of the exact processes involved in the populations described above, it shows that peripheral, relict populations of also widespread species can add valu-able and unique genetic variation. However, these diversifying processes need to act in isolation as homogenizing gene flow from more central parts can signifi-cantly counteract both random processes like genetic drift as well as selective forces.

Despite a study setup that aimed to discriminate between the influence of gene flow and selection in these peripheral and isolated populations additional experi-ments are needed to draw convincing conclusions regarding the opposing alter-natives of swamping gene flow and differing selection pressures. If landscape

274 A. Cassel-Lundhagen

structure is the cause for different phenotypes I would expect a correlation between habitat density and matrix configuration with wing sizes and shapes. If homogeniz-ing gene flow, on the other hand, is causing the observed pattern I would expect the isolated phenotypes to be more successful than the central phenotypes in per-formance experiments in the peripheral region. These hypotheses can be tested and will add important insights into the evolution of peripheral populations and their reactivity to climate change. Further, marginal relict populations constitute ideal study objects of evolution in marginal habitats as they can be used to test how well theory and laboratory experiments reflects more complex natural systems (Kawecki, 2008).

Acknowledgements I thank all co authors and collaborators involved in various parts of the projects. Thanks to Atte Komonen, Ane Laugen and Thomas Schmitt for valuable comments on earlier versions of this manuscript. Part of the data presented here originates from work that was done at the Department of Conservation Biology and Genetics of Uppsala University, Sweden, and at the Department of Biogeography of University of Trier, Germany.

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