Evidence for drought and forest declines during the recent megafaunal extinctions in Madagascar

Aim There remains some uncertainty concerning the causes of extinctions of Madagascar’s megafauna. One hypothesis is that they were caused by over‐hunting by humans. A second hypothesis is that their extinction was caused by both environmental change and hunting. This paper systematically addresses the second hypothesis through examination of two new pollen records from south‐eastern Madagascar alongside other published records across the island. Location South‐eastern Madagascar. Methods We reconstructed past vegetation and fire dynamics over the past 6000 years at two sites in south‐eastern Madagascar (Ste‐Luce) using fossil pollen and charcoal contained in sedimentary sequences. We investigated drivers of vegetation changes and how these, in turn, influenced faunal species in the south‐east, using published climatic, archaeological and faunal records. Further, we also used published records to provide a synthesis of environmental changes on the whole island. Results Vegetation reconstructions indicate that the mosaic vegetation in the region of Ste‐Luce was highly dynamic in response to climatic changes. The open woodland, surrounding the littoral forest, transformed into an ericoid grassland between c. 5800 and 5200 cal. yr bp , possibly in response to a moderate drought recorded during this period. The littoral forest was more stable between c. 5100 and 1000 cal. yr bp , with only some minor compositional changes c. 2800 cal. yr bp and between c. 1900 and 1000 cal. yr bp . Significant forest decline, however, is observed at c. 950 cal. yr bp , coinciding with a drought and a marine surge. A comparison of these results with a synthesis of published vegetation records across the island shows asynchronous vegetation changes in response to various droughts during the Holocene, except for the 950 cal. yr bp drought event, with evidence of widespread vegetation transformations and fires across the island. Main conclusions Pronounced climatic desiccation between 1200 and 700 cal. yr bp may have been the slow driver framing and triggering vegetation transformations and decline in megafaunal populations. In addition, hunting by drought‐impacted human inhabitants and competition with newly introduced cattle would have amplified the impacts on megafaunal populations, leading to numerous extinctions in this period.     

Pleistocene megafaunal extinctions and the functional loss of long‐distance seed‐dispersal services

Pleistocene extinctions affected mainly large‐bodied animals, determining the loss or changes in numerous ecological functions. Evidence points to a central role of many extinct megafauna herbivores as seed dispersers. An important step in understanding the legacy of extinct mutualistic interactions is to evaluate the roles and effectiveness of megafauna herbivores in seed dispersal. Here we use morphological and ecophysiological allometries to estimate both quantitative and qualitative aspects of seed‐dispersal services likely provided by extinct megafauna. We developed a mechanistic model that encompasses four stages of seed dispersal – seed ingestion, gut retention, animal movement, and seed deposition. We estimate seed‐dispersal kernels through simulations to infer the role of Pleistocene megafauna in promoting long‐distance dispersal and examine how seed dispersal was affected by extinctions. Simulations suggest extinct large‐bodied frugivores would frequently disperse large seeds over a thousand meters, whereas smaller‐bodied frugivores are more likely to deposit the seeds over a few hundred meters. Moreover, events of long‐distance seed dispersal by the extinct megafauna would be up to ten times longer than long‐distance dispersal by smaller‐sized extant mammals. By estimating the combined distribution of seed dispersal distances considering all large‐bodied mammalian frugivores in specific South American Pleistocene assemblages we found that long‐distance dispersal contracted by at least two thirds after the megafauna died out. The disruption of long‐distance dispersal is expected to have consequences for recruitment, spatial and genetic structure of plant populations, population persistence and community composition. Promoting long‐distance seed dispersal was one among other salient features of extinct Pleistocene megafauna that reveal their influence on natural ecosystems. Modeling the consequences of megafaunal extinctions can offer quantitative predictions on the consequences of ongoing defaunation to plant populations and ecological communities.     

Genome‐wide scans detect adaptation to aridity in a widespread forest tree species

Patterns of adaptive variation within plant species are best studied through common garden experiments, but these are costly and time‐consuming, especially for trees that have long generation times. We explored whether genome‐wide scanning technology combined with outlier marker detection could be used to detect adaptation to climate and provide an alternative to common garden experiments. As a case study, we sampled nine provenances of the widespread forest tree species, Eucalyptus tricarpa, across an aridity gradient in southeastern Australia. Using a Bayesian analysis, we identified a suite of 94 putatively adaptive (outlying) sequence‐tagged markers across the genome. Population‐level allele frequencies of these outlier markers were strongly correlated with temperature and moisture availability at the site of origin, and with population differences in functional traits measured in two common gardens. Using the output from a canonical analysis of principal coordinates, we devised a metric that provides a holistic measure of genomic adaptation to aridity that could be used to guide assisted migration or genetic augmentation.     

Plant biomes demonstrate that landscape resilience today is the lowest it has been since end‐Pleistocene megafaunal extinctions

Resilient landscapes have helped maintain terrestrial biodiversity during periods of climatic and environmental change. Identifying the tempo and mode of landscape transitions and the drivers of landscape resilience is critical to maintaining natural systems and preserving biodiversity given today's rapid climate and land use changes. However, resilient landscapes are difficult to recognize on short time scales, as perturbations are challenging to quantify and ecosystem transitions are rare. Here we analyze two components of North American landscape resilience over 20,000 years: residence time and recovery time. To evaluate landscape dynamics, we use plant biomes, preserved in the fossil pollen record, to examine how long a biome type persists at a given site (residence time) and how long it takes for the biome at that site to reestablish following a transition (recovery time). Biomes have a median residence time of only 230–460 years. Only 64% of biomes recover their original biome type, but recovery time is 140–290 years. Temperatures changing faster than 0.5°C per 500 years result in much reduced residence times. Following a transition, biodiverse biomes reestablish more quickly. Landscape resilience varies through time. Notably, short residence times and long recovery times directly preceded the end‐Pleistocene megafauna extinction, resulting in regional destabilization, and combining with more proximal human impacts to deliver a one‐two punch to megafauna species. Our work indicates that landscapes today are once again exhibiting low resilience, foreboding potential extinctions to come. Conservation strategies focused on improving both landscape and ecosystem resilience by increasing local connectivity and targeting regions with high richness and diverse landforms can mitigate these extinction risks.     

Climate‐driven ecological stability as a globally shared cause of Late Quaternary megafaunal extinctions: the Plaids and Stripes Hypothesis

Controversy persists about why so many large‐bodied mammal species went extinct around the end of the last ice age. Resolving this is important for understanding extinction processes in general, for assessing the ecological roles of humans, and for conserving remaining megafaunal species, many of which are endangered today. Here we explore an integrative hypothesis that asserts that an underlying cause of Late Quaternary megafaunal extinctions was a fundamental shift in the spatio‐temporal fabric of ecosystems worldwide. This shift was triggered by the loss of the millennial‐scale climate fluctuations that were characteristic of the ice age but ceased approximately 11700 years ago on most continents. Under ice‐age conditions, which prevailed for much of the preceding 2.6 Ma, these radical and rapid climate changes prevented many ecosystems from fully equilibrating with their contemporary climates. Instead of today's ‘striped’ world in which species' ranges have equilibrated with gradients of temperature, moisture, and seasonality, the ice‐age world was a disequilibrial ‘plaid’ in which species' ranges shifted rapidly and repeatedly over time and space, rarely catching up with contemporary climate. In the transient ecosystems that resulted, certain physiological, anatomical, and ecological attributes shared by megafaunal species pre‐adapted them for success. These traits included greater metabolic and locomotory efficiency, increased resistance to starvation, longer life spans, greater sensory ranges, and the ability to be nomadic or migratory. When the plaid world of the ice age ended, many of the advantages of being large were either lost or became disadvantages. For instance in a striped world, the low population densities and slow reproductive rates associated with large body size reduced the resiliency of megafaunal species to population bottlenecks. As the ice age ended, the downsides of being large in striped environments lowered the extinction thresholds of megafauna worldwide, which then increased the vulnerability of individual species to a variety of proximate threats they had previously tolerated, such as human predation, competition with other species, and habitat loss. For many megafaunal species, the plaid‐to‐stripes transition may have been near the base of a hierarchy of extinction causes whose relative importances varied geographically, temporally, and taxonomically.     

Deforestation and apparent extinctions of endemic forest beetles in Madagascar

Madagascar has lost about half of its forest cover since 1953 with much regional variation, for instance most of the coastal lowland forests have been cleared. We sampled the endemic forest-dwelling Helictopleurini dung beetles across Madagascar during 2002-2006. Our samples include 29 of the 51 previously known species for which locality information is available. The most significant factor explaining apparent extinctions (species not collected by us) is forest loss within the historical range of the focal species, suggesting that deforestation has already caused the extinction, or effective extinction, of a large number of insect species with small geographical ranges, typical for many endemic taxa in Madagascar. Currently, roughly 10% of the original forest cover remains. Species-area considerations suggest that this will allow roughly half of the species to persist. Our results are consistent with this prediction.     

A genome‐wide scan for signatures of recent selection in Holstein cattle

The data from the newly available 50 K SNP chip was used for tagging the genome‐wide footprints of positive selection in Holstein–Friesian cattle. For this purpose, we employed the recently described Extended Haplotype Homozygosity test, which detects selection by measuring the characteristics of haplotypes within a single population. To assess formally the significance of these results, we compared the combination of frequency and the Relative Extended Haplotype Homozygosity value of each core haplotype with equally frequent haplotypes across the genome. A subset of the putative regions showing the highest significance in the genome‐wide EHH tests was mapped. We annotated genes to identify possible influence they have in beneficial traits by using the Gene Ontology database. A panel of genes, including FABP3, CLPN3, SPERT, HTR2A5, ABCE1, BMP4 and PTGER2, was detected, which overlapped with the most extreme P‐values. This panel comprises some interesting candidate genes and QTL, representing a broad range of economically important traits such as milk yield and composition, as well as reproductive and behavioural traits. We also report high values of linkage disequilibrium and a slower decay of haplotype homozygosity for some candidate regions harbouring major genes related to dairy quality. The results of this study provide a genome‐wide map of selection footprints in the Holstein genome, and can be used to better understand the mechanisms of selection in dairy cattle breeding.     

Climate change‐driven extinctions of tree species affect forest functioning more than random extinctions

Aim

Climate change affects forest functioning not only through direct physiological effects such as modifying photosynthesis and growing season lengths, but also through indirect effects on community composition related to species extinctions and colonizations. Such indirect effects remain poorly explored in comparison with the direct ones. Biodiversity–ecosystem functioning (BEF) studies commonly examine the effects of species loss by eliminating species randomly. However, species extinctions caused by climate change will depend on the species’ vulnerability to the new environmental conditions, thus occurring in a specific, non‐random order. Here, we evaluated whether successive tree species extinctions, according to their vulnerability to climate change, impact forest functions differently than random species losses.

Location

Eleven temperate forests across a gradient of climatic conditions in central Europe.

Methods

We simulated tree community dynamics with a forest succession model to study the impact of species loss on the communities’ aboveground biomass, productivity and temporal stability. Tree species were removed from the local pool (1) randomly, and according to (2) their inability to be recruited under a warmer climate or (3) their increased mortality under drier conditions.

Results

Results showed that non‐random species loss (i.e., based on their vulnerability to warmer or drier conditions) changed forest functioning at a different rate, and sometimes direction, than random species loss. Furthermore, directed extinctions, unlike random, triggered tipping points along the species loss process where forest functions were strongly impacted. These tipping points occurred after fewer extinctions in forests located in the coldest areas, where ecosystem functioning relies on fewer species.

Main conclusions

We showed that the extinction of species in a deterministic and mechanistically motivated order, in this case the species vulnerability to climate change, strengthens the selection effect of diversity on ecosystem functioning. BEF studies exploring the impact of species loss on ecosystem functioning using random extinctions thus possibly underestimate the potential effect of biodiversity loss when driven by a directional force, such as climate change.

     

Arginine‐ but not alanine‐rich carboxy‐termini trigger nuclear translocation of mutant keratin 10 in ichthyosis with confetti

Ichthyosis with confetti (IWC) is a genodermatosis associated with dominant‐negative variants in keratin 10 (KRT10) or keratin 1 (KRT1). These frameshift variants result in extended aberrant proteins, localized to the nucleus rather than the cytoplasm. This mislocalization is thought to occur as a result of the altered carboxy (C)‐terminus, from poly‐glycine to either a poly‐arginine or ‐alanine tail. Previous studies on the type of C‐terminus and subcellular localization of the respective mutant protein are divergent. In order to fully elucidate the pathomechanism of IWC, a greater understanding is critical. This study aimed to establish the consequences for localization and intermediate filament formation of altered keratin 10 (K10) C‐termini. To achieve this, plasmids expressing distinct KRT10 variants were generated. Sequences encoded all possible reading frames of the K10 C‐terminus as well as a nonsense variant. A keratinocyte line was transfected with these plasmids. Additionally, gene editing was utilized to introduce frameshift variants in exon 6 and exon 7 at the endogenous KRT10 locus. Cellular localization of aberrant K10 was observed via immunofluorescence using various antibodies. In each setting, immunofluorescence analysis demonstrated aberrant nuclear localization of K10 featuring an arginine‐rich C‐terminus. However, this was not observed with K10 featuring an alanine‐rich C‐terminus. Instead, the protein displayed cytoplasmic localization, consistent with wild‐type and truncated forms of K10. This study demonstrates that, of the various 3′ frameshift variants of KRT10, exclusively arginine‐rich C‐termini lead to nuclear localization of K10.     

Environmental heterogeneity and not vicariant biogeographic barriers generate community‐wide population structure in desert‐adapted snakes

Genetic structure can be influenced by local adaptation to environmental heterogeneity and biogeographic barriers, resulting in discrete population clusters. Geographic distance among populations, however, can result in continuous clines of genetic divergence that appear as structured populations. Here, we evaluate the relevant importance of these three factors over a landscape characterized by environmental heterogeneity and the presence of a hypothesized biogeographic barrier in producing population genetic structure within 13 codistributed snake species using a genomic data set. We demonstrate that geographic distance and environmental heterogeneity across western North America contribute to population genomic divergence. Surprisingly, landscape features long thought to contribute to biogeographic barriers play little role in divergence community wide. Our results suggest that isolation by environment is the most important contributor to genomic divergence. Furthermore, we show that models of population clustering that incorporate spatial information consistently outperform nonspatial models, demonstrating the importance of considering geographic distances in population clustering. We argue that environmental and geographic distances as drivers of community‐wide divergence should be explored before assuming the role of biogeographic barriers.     

Local adaptation does not lead to genome‐wide differentiation in lava flow lizards

Adaptation can occur with or without genome‐wide differentiation. If adaptive loci are linked to traits involved in reproductive isolation, genome‐wide divergence is likely, and speciation is possible. However, adaptation can also lead to phenotypic differentiation without genome‐wide divergence if levels of ongoing gene flow are high. Here, we use the replicated occurrence of melanism in lava flow lizards to assess the relationship between local adaptation and genome‐wide differentiation. We compare patterns of phenotypic and genomic divergence among lava flow and nonlava populations for three lizard species and three lava flows in the Chihuahuan Desert. We find that local phenotypic adaptation (melanism) is not typically accompanied by genome‐wide differentiation. Specifically, lava populations do not generally exhibit greater divergence from nonlava populations than expected by geography alone, regardless of whether the lava formation is 5,000 or 760,000 years old. We also infer that gene flow between lava and nonlava populations is ongoing in all lava populations surveyed. Recent work in the isolation by environment and ecological speciation literature suggests that environmentally driven genome‐wide differentiation is common in nature. However, local adaptation may often simply be local adaptation rather than an early stage of ecological speciation.     

Southern montane populations did not contribute to the recolonization of West Siberian Plain by Siberian larch (Larix sibirica): a range‐wide analysis of cytoplasmic markers

While many species were confined to southern latitudes during the last glaciations, there has lately been mounting evidence that some of the most cold‐tolerant species were actually able to survive close to the ice sheets. The contribution of these higher latitude outposts to the main recolonization thrust remains, however, untested. In the present study, we use the first range‐wide survey of genetic diversity at cytoplasmic markers in Siberian larch (Larix sibirica; four mitochondrial (mt) DNA loci and five chloroplast (cp) DNA SSR loci) to (i) assess the relative contributions of southern and central areas to the current L. sibirica distribution range; and (ii) date the last major population expansion in both L. sibirica and adjacent Larix species. The geographic distribution of cpDNA variation was uninformative, but that of mitotypes clearly indicates that the southernmost populations, located in Mongolia and the Tien‐Shan and Sayan Mountain ranges, had a very limited contribution to the current populations of the central and northern parts of the range. It also suggests that the contribution of the high latitude cryptic refugia was geographically limited and that most of the current West Siberian Plain larch populations likely originated in the foothills of the Sayan Mountains. Interestingly, the main population expansion detected through Approximate Bayesian Computation (ABC) in all four larch species investigated here pre‐dates the LGM, with a mode in a range of 220 000–1 340 000 years BP. Hence, L. sibirica, like other major conifer species of the boreal forest, was strongly affected by climatic events pre‐dating the Last Glacial Maximum.     

Pleistocene extinctions and recent expansions in an anguid lizard of the genus Pseudopus

Climatic changes during the Pleistocene played an instrumental role in the shaping recent distribution and diversity of the Western Palearctic biota. Range oscillations often lead to allopatric differentiation followed by the establishment of secondary contact zones. As a result, many species are composed of complex networks of phylogenetic lineages with different histories. Pseudopus apodus is the only surviving member of an ancient genus of Western Palearctic anguid lizards (Anguidae) distributed from the Balkans through Anatolia and Caucasus to central Asia. Here, we used mitochondrial and nuclear DNA sequences to reconstruct the evolutionary history of the species in phylogeographic and demographic frameworks. Our analyses revealed three main phylogenetic lineages that diverged during or shortly before the Pleistocene. Two of them more or less correspond to the known subspecies, and their low genetic variability suggests relatively recent dispersal and colonization of vast parts of the range. The third, southern, lineage is more geographically restricted and diversified than the other two. This pattern shows that the Quaternary climatic oscillations presumably caused repeated large‐scale population extinctions of the species, depleting most of its diversity. Only a few refugia located in Anatolia, Levant, and Transcaucasia served as sources for subsequent recolonization to the areas of the recent distribution. This is in contrast to many other Western Palearctic reptiles that survived unfavorable climatic conditions in numerous local refugia and sanctuaries, which resulted in more complex phylogenetic structure.     

Increased water‐use efficiency during the 20th century did not translate into enhanced tree growth

Aim The goals of this study are: (1) to determine whether increasing atmospheric CO₂ concentrations and changing climate increased intrinsic water use efficiency (iWUE, as detected by changes in Δ¹³C) over the last four decades; and if it did increase iWUE, whether it led to increased tree growth (as measured by tree‐ring growth); (2) to assess whether CO₂ responses are biome dependent due to different environmental conditions, including availability of nutrients and water; and (3) to discuss how the findings of this study can better inform assumptions of CO₂ fertilization and climate change effects in biospheric and climate models. Location A global range of sites covering all major forest biome types. Methods The analysis encompassed 47 study sites including boreal, wet temperate, mediterranean, semi‐arid and tropical biomes for which measurements of tree ring Δ¹³C and growth are available over multiple decades. Results The iWUE inferred from the Δ¹³C analyses of comparable mature trees increased 20.5% over the last 40 years with no significant differences between biomes. This increase in iWUE did not translate into a significant overall increase in tree growth. Half of the sites showed a positive trend in growth while the other half had a negative or no trend. There were no significant trends within biomes or among biomes. Main conclusions These results show that despite an increase in atmospheric CO₂ concentrations of over 50 p.p.m. and a 20.5% increase in iWUE during the last 40 years, tree growth has not increased as expected, suggesting that other factors have overridden the potential growth benefits of a CO₂‐rich world in many sites. Such factors could include climate change (particularly drought), nutrient limitation and/or physiological long‐term acclimation to elevated CO₂. Hence, the rate of biomass carbon sequestration in tropical, arid, mediterranean, wet temperate and boreal ecosystems may not increase with increasing atmospheric CO₂ concentrations as is often implied by biospheric models and short‐term elevated CO₂ experiments.     

Evolvability of between‐year seed dormancy in populations along an aridity gradient

Under global climate change, adaptation to new conditions is crucial for plant species persistence. This requires the ability to evolve in traits that are correlated with changing climatic variables. We studied between‐year seed dormancy, which correlates with environmental variability, and tested for clinal trends in its evolvability along an aridity gradient in Israel. We conducted a germination experiment under five irrigation levels with two dryland winter annuals (Biscutella didyma, Bromus fasciculatus) from four sites along the gradient. Species differed in means and evolvability of dormancy. Biscutella had high dormancy, which significantly increased with aridity but decreased with higher irrigation. In Bromus, dormancy was low, similar among populations, and only marginally affected by irrigation. Evolvability in Biscutella was high and varied among populations, without a clinal trend along the gradient. Conversely, in Bromus, trait evolvability was low and declined with increasing aridity. We argue that changes in evolvability along climatic gradients depend on the relative intensity of stabilizing selection. This may be high in Bromus and not only depends on environmental stress, but also on variability. Our findings point to the importance of measuring evolvability of climate‐related traits across different natural and artificial environments and for many coexisting species. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 924–934.     

Mass extinctions do not explain skew in interspecific body size distributions

In several higher animal taxa, such as mammals and birds, the distribution of species body sizes is heavily skewed towards small size. Previous studies have suggested that small‐bodied organisms are less prone to extinction than large‐bodied species. If small body size is favourable during mass extinction events, a post mass extinction excess of small‐bodied species may proliferate and maintain skewed body size distributions sometime after. Here, we modelled mass extinctions and found that even unrealistically strong body mass selection has little effect on the skew of interspecific body size distributions. Moreover, selection against large body size may, counter intuitively, skew size distributions towards large body size. In any case, subsequent evolutionary diversification rapidly erases these rather small effects mass extinctions may have on size distributions. Next, we used body masses of extant species and phylogenetic methods to investigate possible changes in body size distributions across the Cretaceous–Paleogene (K‐Pg) mass extinction. Body size distributions of extant clades that originated during the Cretaceous are on average more skewed than their subclades that originated during the Paleogene, but the difference is only minor in mammals, and in birds, it can be explained by a positive relationship between species richness and skewness that is also present in clades that originated after the transition. Hence, we cannot infer from extant species whether the K‐Pg mass extinctions were size‐selective, but they are not the reason why most extant bird and mammal species are small‐bodied.