When the pond turtle followed the reindeer: effect of the last extreme global warming event on the timing of faunal change in Northern Europe

Faunal communities have been shaped in different ways by past climatic change. The impact of the termination of the last Glacial and the onset of the present (Holocene) Interglacial on large‐scale faunal shifts, extinction dynamics and gene pools of species are of special interest in natural sciences. A general pattern of climate‐triggered range expansion and local extinction of vertebrate species is known for Europe, and shows that in the modern temperate zone the main faunal change took place mainly during the Late Glacial (14 700–11 700 years ago) and Early Holocene (11 700–9 100 years ago). Based on large datasets of new radiocarbon data, we present precise temporal dynamics of climate‐driven disappearance and appearance of reindeer and pond turtle in southern Sweden. These two species are significant climate indicators in Late Quaternary biostratigraphy. Our data reveal that the reindeer disappeared from southern Sweden ca. 10 300 years ago, whereas the pond turtle colonized the area ca. 9 860 years ago, with a 450‐year gap between each species. This provides evidence for a sudden environmental turnover, causing the replacement of an arctic faunal element by a thermophilic species. The postglacial range dynamics of pond turtle and reindeer are a unique model case, allowing insights into the faunal turnover of other vertebrates during the last dramatic natural global warming event at the Pleistocene–Holocene transition.     

Fossil evidence and phylogeography of temperate species: 'glacial refugia' and post-glacial recolonization

We present a short synthesis of the Pleistocene distribution dynamics and phylogeographic recolonization hypotheses for two temperate European mammal species, the red deer ( Cervus elaphus ) and the roe deer ( Capreolus capreolus ), for which high-resolution patterns of fossil evidence and genetic data sets are available. Such data are critical to an understanding of the role of hypothesized glacial refugia. Both species show a similar pattern: a relatively wide distribution in the southern part of Central Europe 60,000–25,000 years ago, and a strong restriction to areas in southern Europe for nearly 10,000 years during the Last Glacial Maximum (LGM) and the early Late Glacial (25,000–14,700 years ago). With the beginning of Greenland Interstadial 1 (Bølling/Allerød warming, c. 14,700–11,600 years ago) a sudden range expansion into Central Europe is visible, but the colonization of most of Central Europe, including the northern European Lowlands, only began in the early Holocene. In a European context, regions where the species were distributed during the LGM and early Late Glacial are most relevant as potential origins of recolonization processes, because during these c. 10,000 years distribution ranges were smaller than at any other time in the Late Quaternary. As far as the present distribution of temperate species and their genetic lineages is concerned, so-called 'cryptic refugia' are important only if the species are actually confirmed there during the LGM, as otherwise they could not possibly have contributed to the recolonization that eventually resulted in the present distribution ranges.     

Rapid divergence in physiological and life-history traits between northern and southern populations of the British introduced neo-species, Senecio squalidus

Alien plants provide a unique opportunity to study evolution in novel environments, but relatively little is known about the extent to which they become locally adapted to different environments across their new range. Here, we compare northern and southern populations of the introduced species Senecio squalidus in Britain; S. squalidus has been in southern Britain for approximately 200  years and reached Scotland only about 50  years ago. We conducted common garden experiments at sites in the north and south of the species' range in Britain. We also conducted glasshouse and growth chamber experiments to test the hypothesis that southern genotypes flower later, are more drought-tolerant, germinate and establish better at warmer temperatures, and are less sensitive to cold stress than their more northern counterparts. Results from the common garden experiments are largely consistent with the hypothesis of rapid adaptive divergence of populations of the species within the introduced range, with genotypes typically showing a home-site advantage. Results from the glasshouse and growth chamber experiments demonstrate adaptive divergence in ability to tolerate drought stress and high temperatures, as well as in phenology. In particular, southern genotypes were more tolerant of dry conditions and high temperatures and they flowered later than northern genotypes. Our results show that rapid local adaptation can occur in alien species, and they have implications for our understanding of the ecological genetics of range expansion of introduced weeds.     

Ancient DNA identifies post‐glacial recolonisation,not recent bottlenecks,as the primary driver of contemporary mtDNA phylogeography and diversity in Scandinavian brown bears

Aim

Brown bear populations in Scandinavia show a strong mitochondrial DNA (mtDNA) phylogeographic structure and low diversity relative to other parts of Europe. Identifying the timing and origins of this mtDNA structure is important for conservation programs aimed at restoring populations to a natural state. Therefore, it is essential to identify whether contemporary genetic structure is linked to post‐glacial recolonisation from divergent source populations or an artefact of demographic impacts during recent population bottlenecks. We employed ancient DNA techniques to investigate the timing and potential causes of these patterns.

Location

Scandinavia and Europe.

Methods

Ancient mtDNA sequences from 20 post‐glacial Scandinavian bears were used to investigate phylogeographic structure and genetic diversity over the last 6000 years. MtDNA from 19 Holocene Norwegian bears was compared with 499 sequences from proximate extant populations in Sweden, Finland, Estonia and western Russia. A single mtDNA sequence from a Holocene Denmark sample was compared with 149 ancient and modern bears from Western Europe.

Results

All nineteen Holocene Norwegian samples are identical to or closely related to the most common mtDNA haplotype found in northern Europe today. MtDNA diversity was low and not significantly different from extant populations in northern Europe. In Denmark, we identified a single mtDNA haplotype that is previously unrecorded from Scandinavia.

Main conclusions

The current discrete phylogeographic structure and lack of mtDNA diversity in Scandinavia is attributed to serial founder effects during post‐glacial recolonisation from divergent source populations rather than an artefact of recent anthropogenic impacts. In contrast to previous interpretations, the recolonisation of southern Scandinavia may not have been limited to bears from a single glacial refugium. Results highlight the importance of conserving the long‐term evolutionary separation between northern and southern populations and identify southern Scandinavia as an important reservoir of mtDNA diversity that is under threat in other parts of Europe.

     

Where are you from,stranger? The enigmatic biogeography of North African pond turtles (Emys orbicularis)

The European pond turtle (Emys orbicularis) is a Nearctic element in the African fauna and thought to have invaded North Africa from the Iberian Peninsula. All North African populations are currently identified with the subspecies E. o. occidentalis. However, a nearly range-wide sampling in North Africa used for analyses of mitochondrial and microsatellite DNA provides evidence that only Moroccan populations belong to this taxon, while eastern Algerian and Tunisian pond turtles represent an undescribed distinct subspecies. These two taxa are most closely related to E. o. galloitalica with a native distribution along the Mediterranean coast of northern Spain through southern France to western and southern Italy. This group is sister to a clade comprising several mitochondrial lineages and subspecies of E. orbicularis from Central and Eastern Europe plus Asia, and the successive sisters are E. o. hellenica and E. trinacris. Our results suggest that E. orbicularis has been present in North Africa longer than on the Iberian Peninsula and that after an initial invasion of North Africa by pond turtles from an unknown European source region, there was a phase of diversification in North Africa, followed by a later re-invasion of Europe by one of the African lineages. The differentiation of pond turtles in North Africa parallels a general phylogeographic paradigm in amphibians and reptiles, with deeply divergent lineages in the western and eastern Maghreb. Acknowledging their genetic similarity, we propose to synonymize the previously recognized Iberian subspecies E. o. fritzjuergenobsti with E. o. occidentalis sensu stricto. The seriously imperiled Moroccan populations of E. o. occidentalis represent two Management Units different in mitochondrial haplotypes and microsatellite markers. The conservation status of eastern Algerian pond turtles is unclear, while Tunisian populations are endangered. Considering that Algerian and Tunisian pond turtles represent an endemic taxon, their situation throughout the historical range should be surveyed to establish a basis for conservation measures.     

Late Quaternary history of Hippophaë rhamnoides L. (Elaeagnaceae) inferred from chalcone synthase intron (Chsi) sequences and chloroplast DNA variation

Fossil pollen records indicate that Hippophaë rhamnoides (Sea Buckthorn) was widespread on late‐ and early postglacial raw soils throughout much of central and northern Europe, but that Early Holocene reforestation restricted populations to northern coastal habitats, or along mountain streams in the Alps, Pyrenees, and Carpathians. We used sequence variation at the nuclear chalcone synthase intron (Chsi), in conjunction with chloroplast DNA–restriction fragment length polymorphism data, to investigate the intraspecific phylogeny, phylogeographic structure, and expansion demographic history of this dioecious and wind‐pollinated shrub at its range‐wide scale in Europe and Asia Minor. Four major Chsi phylogroups of unresolved relationships were identified with estimated divergences ～172 000 years ago. Large‐scale phylogeographic structures of nuclear and cytoplasmic markers were congruent in identifying (i) southeastern Europe as the most likely source of colonization into central Europe and Scandinavia, and (ii) the area just north of the Alps as a contact zone between populations from the Alps and the east/central European‐Scandinavian lineage. Coalescence‐based analyses (i.e. nested clade analysis and mismatch distributions) of Chsi variation were able to detect at least four major episodes of population growth, all within about the last 40 000 years. In particular, these analyses identified a nearly synchronized timing of population expansions in various parts of the species’ range in central‐eastern Europe/Asia Minor, most likely correlating with the Younger Dryas Stadial (～13 000–11 600 years ago). It remains to be established whether the phylogeographic history of H. rhamnoides, and particularly its rapid response to the rapid environmental changes of the Younger Dryas cold snap, is unique to the species, or whether it is shared with other cold‐tolerant shrub (or grassland) species known from late‐glacial raw soils in Europe.     

Evidence of counter‐gradient growth in western pond turtles (Actinemys marmorata) across thermal gradients

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Speciation in Pararge (Satyrinae: Nymphalidae) butterflies – North Africa is the source of ancestral populations of all Pararge species

Abstract.  The genus Pararge comprises three species: P. aegeria , distributed in Europe and North Africa; P. xiphia , endemic to Madeira; and P. xiphioides , endemic to the Canary Islands. Two subspecies are recognized in P. aegeria , P. a. tircis and P. a. aegeria , distributed in northern and southern Europe, respectively. In the 1970s, P. aegeria appeared on Madeira. However, despite the status of P. aegeria as a model species in ecological studies, the evolutionary history of Pararge remains unknown. We studied the phylogenetic relationships of the three Pararge species, using the mitochondrial gene cytochrome oxidase subunit I and the nuclear gene wingless to infer modes and times of speciation. On the basis of our analyses, Pararge forms a strongly supported monophyletic group, with the DNA haplotypes of the three species also forming well-supported monophyletic groups. We found that P. xiphia diverged first from the common ancestor a maximum of five million years ago, with P. xiphioides and P. aegeria being sister species that diverged a maximum of three million years ago. The two subspecies, P. a. tircis and P. a. aegeria , were not distinguishable on the basis of DNA haplotypes; instead, our data clearly distinguished between European specimens and those from North Africa. Madeiran P. aegeria has North African haplotypes and thus originated from there rather than from Europe. We hypothesize that the Mediterranean Sea forms a strong barrier to dispersal for Pararge butterflies, and has done so for approximately the past one million years.     

Late‐glacial recolonization and phylogeography of European red deer (Cervus elaphus L.)

The Pleistocene was an epoch of extreme climatic and environmental changes. How individual species responded to the repeated cycles of warm and cold stages is a major topic of debate. For the European fauna and flora, an expansion–contraction model has been suggested, whereby temperate species were restricted to southern refugia during glacial times and expanded northwards during interglacials, including the present interglacial (Holocene). Here, we test this model on the red deer (Cervus elaphus) a large and highly mobile herbivore, using both modern and ancient mitochondrial DNA from the entire European range of the species over the last c. 40 000 years. Our results indicate that this species was sensitive to the effects of climate change. Prior to the Last Glacial Maximum (LGM) haplogroups restricted today to South‐East Europe and Western Asia reached as far west as the UK. During the LGM, red deer was mainly restricted to southern refugia, in Iberia, the Balkans and possibly in Italy and South‐Western Asia. At the end of the LGM, red deer expanded from the Iberian refugium, to Central and Northern Europe, including the UK, Belgium, Scandinavia, Germany, Poland and Belarus. Ancient DNA data cannot rule out refugial survival of red deer in North‐West Europe through the LGM. Had such deer survived, though, they were replaced by deer migrating from Iberia at the end of the glacial. The Balkans served as a separate LGM refugium and were probably connected to Western Asia with genetic exchange between the two areas.     

When east met west: the sub-fossil footprints of the west European hedgehog and the northern white-breasted hedgehog during the Late Quaternary in Europe

The distinct distribution of the west European hedgehog Erinaceus europaeus and the northern white-breasted hedgehog Erinaceus roumanicus and their separate refugial origins after the Pleistocene is a well-known example in the zoogeography of the Holarctic. Among the Late Quaternary faunal assemblages, the west European hedgehog is recorded at 269 sites whereas the northern white-breasted hedgehog is recorded only at 52 sites in Europe. The distribution patterns of the temporal and spatial Glacial records of the west European hedgehog show a general trend: a strong restriction to glacial refugia (the Iberian and Italian Peninsulas) during the Weichselian Glacial until the end of the Last Glacial Maximum, and a colonization of southern France during the early Late Glacial between 14 000 and 125 00 ¹⁴C years BP (15 000–12 800 cal. BC). Whereas the British Isles could have already been colonised by the end of the Pre-Boreal, in the rest of Central Europe E. europaeus was clearly distributed there in the Boreal for the first time. The west European hedgehog is an absolute Holocene faunal element in Central Europe. It appears in most parts of Central Europe during the Early Holocene, when the west European hedgehog met its eastern relative, which probably was similarly sensitive. After meeting each other, the distribution limit of both Erinaceus species in Central Europe seems to have been relatively constant in its geographic extent. Because of the clear climatic correlation, E. europaeus should be considered as an indicator species for temperate climatic conditions of the Holocene fauna. This should be considered during the reconstruction of climatic conditions with the help of the analysis of quaternary faunal material.     

Mitochondrial and microsatellite DNA markers reveal a Balkan origin for the highly invasive horse-chestnut leaf miner Cameraria ohridella (Lepidoptera, Gracillariidae)

Biological invasions usually start with a small number of founder individuals. These founders are likely to represent a small fraction of the total genetic diversity found in the source population. Our study set out to trace genetically the geographical origin of the horse-chestnut leafminer, Cameraria ohridella , an invasive microlepidopteran whose area of origin is still unkown. Since its discovery in Macedonia 25 years ago, this insect has experienced an explosive westward range expansion, progressively colonizing all of Central and Western Europe. We used cytochrome oxidase I sequences (DNA barcode fragment) and a set of six polymorphic microsatellites to assess the genetic variability of C. ohridella populations, and to test the hypothesis that C. ohridella derives from the southern Balkans (Albania, Macedonia and Greece). Analysis of mtDNA of 486 individuals from 88 localities allowed us to identify 25 geographically structured haplotypes. In addition, 480 individuals from 16 populations from Europe and the southern Balkans were genotyped for 6 polymorphic microsatellite loci. High haplotype diversity and low measures of nucleotide diversities including a significantly negative Tajima's D indicate that C. ohridella has experienced rapid population expansion during its dispersal across Europe. Both mtDNA and microsatellites show a reduction in genetic diversity of C. ohridella populations sampled from artificial habitats (e.g. planted trees in public parks, gardens, along roads in urban or sub-urban areas) across Europe compared with C. ohridella sampled in natural stands of horse-chestnuts in the southern Balkans. These findings suggest that European populations of C. ohridella may indeed derive from the southern Balkans.     

A new cryptic species of pond turtle from southern Italy, the hottest spot in the range of the genus Emys (Reptilia, Testudines, Emydidae)

Geographic variation in the mtDNA haplotypes (cytochrome b gene) of 127 European pond turtles from Italy was investigated. Thirty‐eight of the Italian samples were also studied by nuclear fingerprinting (ISSR PCR) and compared with samples from other parts of the range representing all nine currently known mtDNA lineages of Emys orbicularis. Our genetic findings were compared against morphological data sets (measurements, colour pattern) for 109 adult turtles from southern Italy. Italy is displaying on a small geographical scale the most complicated variation known over the entire distributional area of Emys (North Africa over Europe and Asia Minor to the Caspian and Aral Seas). The Tyrrhenic coast of the Apennine Peninsula, the Mt. Pollino area and Basilicata are inhabited by Emys orbicularis galloitalica, a subspecies harbouring a distinct mtDNA lineage. The same lineage is also found in Sardinia. Along the Adriatic coast of Italy and on the Salentine Peninsula (Apulia, southern Italy), another morphologically distinctive subspecies (Emys orbicularis hellenica) occurs, which also bears a different mtDNA lineage. A higher diversity of mtDNA haplotypes in the south of the Apennine Peninsula suggests that the glacial refugia of E. o. galloitalica and E. o. hellenica were located here. A further refuge of E. o. hellenica probably existed in the southern Balkans. The west coasts of the Balkans and Corfu have probably been colonized from Italy and not from the geographically closer southern Balkanic refuge. In Sicily, a third mtDNA lineage is distributed, which is sister to all other known lineages of Emys. Morphologically, Sicilian pond turtles resemble E. o. galloitalica. However, nuclear fingerprinting revealed a clear distinctiveness of the Sicilian taxon, whereas no significant divergence was detected between representatives of the other eight mtDNA lineages of Emys. Furthermore, nuclear fingerprinting provided no evidence for current or past gene flow between the Sicilian taxon and the mainland subspecies of E. orbicularis. Therefore, Sicilian pond turtles are described here as a species new to science. Some populations in Calabria and on the Salentine Peninsula comprise individuals of different mtDNA lineages. We interpret this as a natural contact. However, we cannot exclude that these syntopic occurrences are the result of human activity. For example, in other parts of Italy, the natural distribution pattern of Emys is obscured by allochthonous turtles. This could also be true for southern Italy. The discovery of the complex taxonomic differentiation in southern Italy requires reconsidering conservation strategies.