Arndt Hampe

Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations

Plants offer excellent models to investigate how gene flow shapes the organization of genetic diversity. Their three genomes can have different modes of transmission and will hence experience varying levels of gene flow. We have compiled studies of genetic structure based on chloroplast DNA (cpDNA), mitochondrial DNA (mtDNA) and nuclear markers in seed plants. Based on a data set of 183 species belonging to 103 genera and 52 families, we show that the precision of estimates of genetic differentiation (GST) used to infer gene flow is mostly constrained by the sampling of populations. Mode of inheritance appears to have a major effect on GST. Maternally inherited genomes experience considerably more subdivision (median value of 0.67) than paternally or biparentally inherited genomes (∼0.10). GST at cpDNA and mtDNA markers covary narrowly when both genomes are maternally inherited, whereas GST at paternally and biparentally inherited markers also covary positively but more loosely and GST at maternally inherited markers are largely independent of values based on nuclear markers. A model‐based gross estimate suggests that, at the rangewide scale, historical levels of pollen flow are generally at least an order of magnitude larger than levels of seed flow (median of the pollen‐to‐seed migration ratio: 17) and that pollen and seed gene flow vary independently across species. Finally, we show that measures of subdivision that take into account the degree of similarity between haplotypes (NST or RST) make better use of the information inherent in haplotype data than standard measures based on allele frequencies only.

INVITED REVIEW: Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations

Plants offer excellent models to investigate how gene flow shapes the organization of genetic diversity. Their three genomes can have different modes of transmission and will hence experience varying levels of gene flow. We have compiled studies of genetic structure based on chloroplast DNA (cpDNA), mitochondrial DNA (mtDNA) and nuclear markers in seed plants. Based on a data set of 183 species belonging to 103 genera and 52 families, we show that the precision of estimates of genetic differentiation (GST) used to infer gene flow is mostly constrained by the sampling of populations. Mode of inheritance appears to have a major effect on GST. Maternally inherited genomes experience considerably more subdivision (median value of 0.67) than paternally or biparentally inherited genomes (∼0.10). GST at cpDNA and mtDNA markers covary narrowly when both genomes are maternally inherited, whereas GST at paternally and biparentally inherited markers also covary positively but more loosely and GST at maternally inherited markers are largely independent of values based on nuclear markers. A model‐based gross estimate suggests that, at the rangewide scale, historical levels of pollen flow are generally at least an order of magnitude larger than levels of seed flow (median of the pollen‐to‐seed migration ratio: 17) and that pollen and seed gene flow vary independently across species. Finally, we show that measures of subdivision that take into account the degree of similarity between haplotypes (NST or RST) make better use of the information inherent in haplotype data than standard measures based on allele frequencies only.

Can Population Genetic Structure Be Predicted from Life-History Traits?

Population genetic structure is a key parameter in evolutionary biology. Earlier comparative studies have shown that genetic structure depends on species ecological attributes and life‐history traits, but species phylogenetic relatedness had not been accounted for. Here we reevaluate the relationships between genetic structure and species traits in seed plants. Each species is characterized by a set of life‐history and ecological features as well as by its geographic range size, its heterozygote deficit, and its genetic structure at nuclear and organelle markers to distinguish between pollen‐ and seed‐mediated gene flow. We use both a conventional regression approach and a method that controls for phylogenetic relationships. Once phylogenetic conservatism and covariation among traits are taken into account, genetic structure is shown to be related with only a few synthetic traits, such as mating system for nuclear markers and seed dispersal mode or geographic range size for organelle markers. Along with other studies on invasiveness or rarity, our work illustrates the fact that predicting the fate of species across a broad taxonomic assemblage on the basis of simple traits is rarely possible, a testimony of the highly contingent nature of evolution.

Climate refugia: joint inference from fossil records, species distribution models and phylogeography

Climate refugia, locations where taxa survive periods of regionally adverse climate, are thought to be critical for maintaining biodiversity through the glacial-interglacial climate changes of the Quaternary. A critical research need is to better integrate and reconcile the three major lines of evidence used to infer the existence of past refugia - fossil records, species distribution models and phylogeographic surveys - in order to characterize the complex spatiotemporal trajectories of species and populations in and out of refugia. Here we review the complementary strengths, limitations and new advances for these three approaches. We provide case studies to illustrate their combined application, and point the way towards new opportunities for synthesizing these disparate lines of evidence. Case studies with European beech, Qinghai spruce and Douglas-fir illustrate how the combination of these three approaches successfully resolves complex species histories not attainable from any one approach. Promising new statistical techniques can capitalize on the strengths of each method and provide a robust quantitative reconstruction of species history. Studying past refugia can help identify contemporary refugia and clarify their conservation significance, in particular by elucidating the fine-scale processes and the particular geographic locations that buffer species against rapidly changing climate.

Rangewide phylogeography of a bird-dispersed Eurasian shrub: contrasting Mediterranean and temperate glacial refugia.

We studied the phylogeography of alder buckthorn (Frangula alnus), a bird‐dispersed shrub or small tree distributed over most of Europe and West Asia and present in three of the four main refugia of West Palaearctic temperate woody plants: the Iberian Peninsula, the Balkans and Anatolia. A total of 78 populations from 21 countries were analysed for chloroplast DNA variation using polymerase chain reaction–restriction fragment length polymorphism (PCR–RFLP), and 21 different haplotypes were distinguished. We found a very strong overall population differentiation (GST = 0.81) and phylogeographical structure, and a sharp contrast between the haplotype‐rich refugia and the almost completely uniform area of postglacial colonization. The haplotype network comprises three lineages made up of haplotypes from the Iberian Peninsula, Anatolia with the Caucasus, and temperate Europe. The Iberian and the Anatolian branches represent parts of a major lineage that spans over the whole northern Mediterranean Basin and some neighbouring areas and probably dates back to the Tertiary. Many haplotypes of this lineage are distributed locally and most populations are fixed for a single haplotype; these populations have apparently been very stable since their establishment, experiencing negligible gene flow and few mutations. The temperate European lineage consists of one very widespread and abundant plus six locally distributed haplotypes. Four of them are located in Southeast Europe, the putative refugium of all extant temperate European populations. Contrary to populations from Iberia and Anatolia, F. alnus populations from the southeastern European refugium have most genetic variation within populations. Bird‐mediated seed dispersal has apparently allowed not only a very rapid postglacial expansion of F. alnus but also subsequent regular seed exchanges between populations of the largely continuous species range in temperate Europe. In contrast, the disjunct F. alnus populations persisting in Mediterranean mountain ranges seem to have experienced little gene flow and have therefore accumulated a high degree of differentiation, even at short distances. Populations from the southern parts of the glacial refugia have contributed little to the postglacial recolonization of Europe, but their long‐term historical continuity has allowed them to maintain a unique store of genetic variation.

Paleoecology meets genetics: deciphering past vegetational dynamics

Abstract Genetic analysis adds a novel dimension to paleoecology that is becoming increasingly important for elucidating vegetational dynamics in relation to climate change. Because past vegetational changes have often left distinct genetic imprints on current plant populations, genetic analysis can add detail to fossil-based reconstructions. Recent surveys of DNA polymorphisms yield new insights into past vegetational changes and address long-standing paleoecological questions. These studies reveal that small tree populations survived in mid- to high-latitude refugia throughout the Quaternary glacial episodes. They further reveal migration pathways and demographic processes during postglacial range expansion. These results challenge previous notions regarding tree species responses to climate change and help to identify genetic conservation targets. Here, we review these recent advances and outline research prospects at the interface between paleoecology and genetics.

INVITED REVIEW: Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations: ORGANIZATION OF GENETIC DIVERSITY IN PLANTS

Plants offer excellent models to investigate how gene flow shapes the organization of genetic diversity. Their three genomes can have different modes of transmission and will hence experience varying levels of gene flow. We have compiled studies of genetic structure based on chloroplast DNA (cpDNA), mitochondrial DNA (mtDNA) and nuclear markers in seed plants. Based on a data set of 183 species belonging to 103 genera and 52 families, we show that the precision of estimates of genetic differentiation (GST) used to infer gene flow is mostly constrained by the sampling of populations. Mode of inheritance appears to have a major effect on GST. Maternally inherited genomes experience considerably more subdivision (median value of 0.67) than paternally or biparentally inherited genomes (∼0.10). GST at cpDNA and mtDNA markers covary narrowly when both genomes are maternally inherited, whereas GST at paternally and biparentally inherited markers also covary positively but more loosely and GST at maternally inherited markers are largely independent of values based on nuclear markers. A model‐based gross estimate suggests that, at the rangewide scale, historical levels of pollen flow are generally at least an order of magnitude larger than levels of seed flow (median of the pollen‐to‐seed migration ratio: 17) and that pollen and seed gene flow vary independently across species. Finally, we show that measures of subdivision that take into account the degree of similarity between haplotypes (NST or RST) make better use of the information inherent in haplotype data than standard measures based on allele frequencies only.

Recruitment and regeneration in populations of an endangered South Iberian Tertiary relict tree

The southern Iberian Peninsula is one of the most important refugia of Tertiary relict plant taxa in Europe. Under the present summer-dry climate, relict populations may experience a severely reduced regeneration. We studied the demographic structure, seed set and initial recruitment in relict populations of the endangered tree Frangula alnus subsp. baetica (Rhamnaceae) to evaluate its regeneration potential under the present environmental conditions. Populations are restricted to small riparian forests of Southwest Spanish and North Moroccan mountain ranges. The distribution of fruit crop sizes was highly left-skewed, and a few old trees produced the large bulk of the population seed pool. Bird-mediated seed dispersal appeared inefficient and post-dispersal seed predation by mice was high. Secondary seed transport by elevated creek water flow after winter rains modified the primary seed dispersal, but in consequence most seeds germinated on recently formed sandbanks where seedlings experienced reduced initial growth and survival. The most important mortality factor was desiccation, followed by herbivory. None of 1144 monitored seedlings survived for 2 years. The demographic survey through five populations indicates that drought periods may cause temporal regeneration bottlenecks. Moreover, over the last two decades populations have experienced increasing regeneration problems. Two causes are suggested: (1) browsing pressure from introduced game animals, and (2) the impact of torrential water flow peaks after heavy winter rains, exacerbated by large-scale vegetation slashing in surrounding cork oak forests. We discuss conservation strategies for this and other relict tree species that account for the pecularities of their habitat within the Mediterranean.

Origin of spatial genetic structure in an expanding oak population.

Spatial genetic structure (SGS) results from the interplay of several demographical processes that are difficult to tease apart. In this study, we explore the specific effects of seed and pollen dispersal and of early postdispersal mortality on the SGS of a seedling cohort (N = 786) recruiting within and around an expanding pedunculate oak (Quercus robur) stand. Using data on dispersal (derived from parentage analysis) and mortality (monitored in the field through two growing seasons), we decompose the overall SGS of the cohort into its components by contrasting the SGS of dispersed (i.e. growing away from their mother tree) vs. nondispersed (i.e. growing beneath their mother tree) and initial vs. surviving seedlings. Patterns differ strongly between nondispersed and dispersed seedlings. Nondispersed seedlings are largely responsible for the positive kinship values observed at short distances in the studied population, whereas dispersed seedlings determine the overall SGS at distances beyond c. 30 m. The paternal alleles of nondispersed seedlings show weak yet significantly positive kinships up to c. 15 m, indicating some limitations in pollen flow that should further promote pedigree structures at short distances. Seedling mortality does not alter SGS, except for a slight increase in the nondispersed group. Field data reveal that mortality in this group is negatively density‐dependent, probably because of small‐scale variation in light conditions. Finally, we observe a remarkable similarity between the SGS of the dispersed seedlings and that of the adults, which probably reflects dispersal processes during the initial expansion of the population. Overall, this study demonstrates that incorporating individual‐level complementary information into analyses can greatly improve the detail and confidence of ecological inferences drawn from SGS.

Climate refugia: from the Last Glacial Maximum to the twenty‐first century

ThehistoryofEarth is ahistoryof recurrent climate change.Today’s globalbiodiversitydemonstrates thatmany specieshavebeenable to cope with climate shifts in the past. Yet great concern exists that modern climate change is likely to overstrain the capacity of many species to track suitable climate spaces, potentially leading to widespread extinctions through the coming decades. This view is further promoted by a large number of species distribution modeling (SDM) forecasts. It remains, however, relatively little appreciated that the deeply troubling picture stands in contrast to empirical records of species responses to past climatic changes (Botkin et al., 2007). Fossil data indicate that extensive range dynamics andmassive community reshuffling occurred during past periods of rapid climate transitions. But, at least for plants, there is little evidence that pastmajorwarming eventswere accompaniedby increased global-scale extinction rates (Willis & MacDonald, 2011). One possible explanation for this apparent contradiction is that climate refugia – areas where local populations of a species can persist throughperiods of unfavorable regional climate– could have beenmuchmore commonandwidespread thanpreviously thought. Such areas would have helped sustain regional biodiversity through periodsofadverseclimateormajorclimatic transitions, andservedas sources for the subsequent re-expansion of confined populations. The existence and identification of refugia during the Last Glacial Maximum (c. 19–26 kyr BP; Clark et al., 2009) has been a topic of active research for decades. Recent evidence indicates that many temperate and boreal species have maintained populations at considerably higher latitudes than previously assumed (Hu et al., 2009;Mosblech et al., 2011). Such locations are commonly referred to as ‘cryptic refugia’, a term that nicely conveys the difficulties in inferring the past existence of these small and scattered refugial populations. The crucial role of climate refugia for the long-term maintenance of regional to global biodiversity, and the growing awareness that refugia may be similarly relevant as ‘safe havens’ under future climate warming, have sparked great interest in their identification and functioning (e.g. M edail & Diadema, 2009; Stewart et al., 2010; Keppel et al., 2012). Joining research perspectives and approaches