Nicholas J. Matzke

Has the Earth’s sixth mass extinction already arrived?

Palaeontologists characterize mass extinctions as times when the Earth loses more than three-quarters of its species in a geologically short interval, as has happened only five times in the past 540 million years or so. Biologists now suggest that a sixth mass extinction may be under way, given the known species losses over the past few centuries and millennia. Here we review how differences between fossil and modern data and the addition of recently available palaeontological information influence our understanding of the current extinction crisis. Our results confirm that current extinction rates are higher than would be expected from the fossil record, highlighting the need for effective conservation measures.

Approaching a state shift in Earth’s biosphere

Localized ecological systems are known to shift abruptly and irreversibly from one state to another when they are forced across critical thresholds. Here we review evidence that the global ecosystem as a whole can react in the same way and is approaching a planetary-scale critical transition as a result of human influence. The plausibility of a planetary-scale ‘tipping point’ highlights the need to improve biological forecasting by detecting early warning signs of critical transitions on global as well as local scales, and by detecting feedbacks that promote such transitions. It is also necessary to address root causes of how humans are forcing biological changes.

Model Selection in Historical Biogeography Reveals that Founder-Event Speciation Is a Crucial Process in Island Clades

Founder-event speciation, where a rare jump dispersal event founds a new genetically isolated lineage, has long been considered crucial by many historical biogeographers, but its importance is disputed within the vicariance school. Probabilistic modeling of geographic range evolution creates the potential to test different biogeographical models against data using standard statistical model choice procedures, as long as multiple models are available. I re-implement the Dispersal-Extinction-Cladogenesis (DEC) model of LAGRANGE in the R package BioGeoBEARS, and modify it to create a new model, DEC + J, which adds founder-event speciation, the importance of which is governed by a new free parameter, [Formula: see text]. The identifiability of DEC and DEC + J is tested on data sets simulated under a wide range of macroevolutionary models where geography evolves jointly with lineage birth/death events. The results confirm that DEC and DEC + J are identifiable even though these models ignore the fact that molecular phylogenies are missing many cladogenesis and extinction events. The simulations also indicate that DEC will have substantially increased errors in ancestral range estimation and parameter inference when the true model includes + J. DEC and DEC + J are compared on 13 empirical data sets drawn from studies of island clades. Likelihood-ratio tests indicate that all clades reject DEC, and AICc model weights show large to overwhelming support for DEC + J, for the first time verifying the importance of founder-event speciation in island clades via statistical model choice. Under DEC + J, ancestral nodes are usually estimated to have ranges occupying only one island, rather than the widespread ancestors often favored by DEC. These results indicate that the assumptions of historical biogeography models can have large impacts on inference and require testing and comparison with statistical methods.

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.

Treating Fossils as Terminal Taxa in Divergence Time Estimation Reveals Ancient Vicariance Patterns in the Palpimanoid Spiders

Incorporation of fossils into biogeographic studies can have a profound effect on the conclusions that result, particularly when fossil ranges are nonoverlapping with extant ranges. This is the case in archaeid spiders, where there are known fossils from the Northern Hemisphere, yet all living members are restricted to the Southern Hemisphere. To better understand the biogeographic patterns of archaeid spiders and their palpimanoid relatives, we estimate a dated phylogeny using a relaxed clock on a combined molecular and morphological data set. Dating information is compared with treating the archaeid fossil taxa as both node calibrations and as noncontemporaneous terminal tips, both with and without additional calibration points. Estimation of ancestral biogeographic ranges is then performed, using likelihood and Bayesian methods to take into account uncertainty in phylogeny and in dating. We find that treating the fossils as terminal tips within a Bayesian framework, as opposed to dating the phylogeny based only on molecular data with the dates coming from node calibrations, removes the subjectivity involved in assigning priors, which has not been possible with previous methods. Our analyses suggest that the diversification of the northern and southern archaeid lineages was congruent with the breakup of Pangaea into Laurasia and Gondwanaland. This analysis provides a rare example, and perhaps the most strongly supported, where a dated phylogeny confirms a biogeographical hypothesis based on vicariance due to the breakup of the ancient continental plates.

The incidence and implications of clouds for cloud forest plant water relations

Although clouds are the most recognisable and defining feature of tropical montane cloud forests, little research has focussed on how clouds affect plant functioning. We used satellite and ground-based observations to study cloud and leaf wetting patterns in contrasting tropical montane and pre-montane cloud forests. We then studied the consequences of leaf wetting for the direct uptake of water accumulated on leaf surfaces into the leaves themselves. During the dry season, the montane forest experienced higher precipitation, cloud cover and leaf wetting events of longer duration than the pre-montane forest. Leaf wetting events resulted in foliar water uptake in all species studied. The capacity for foliar water uptake differed significantly between the montane and pre-montane forest plant communities, as well as among species within a forest. Our results indicate that foliar water uptake is common in these forest plants and improves plant water status during the dry season.

Whole mitochondrial genome sequencing of domestic horses reveals incorporation of extensive wild horse diversity during domestication

BackgroundDNA target enrichment by micro-array capture combined with high throughput sequencing technologies provides the possibility to obtain large amounts of sequence data (e.g. whole mitochondrial DNA genomes) from multiple individuals at relatively low costs. Previously, whole mitochondrial genome data for domestic horses (Equus caballus) were limited to only a few specimens and only short parts of the mtDNA genome (especially the hypervariable region) were investigated for larger sample sets.ResultsIn this study we investigated whole mitochondrial genomes of 59 domestic horses from 44 breeds and a single Przewalski horse (Equus przewalski) using a recently described multiplex micro-array capture approach. We found 473 variable positions within the domestic horses, 292 of which are parsimony-informative, providing a well resolved phylogenetic tree. Our divergence time estimate suggests that the mitochondrial genomes of modern horse breeds shared a common ancestor around 93,000 years ago and no later than 38,000 years ago. A Bayesian skyline plot (BSP) reveals a significant population expansion beginning 6,000-8,000 years ago with an ongoing exponential growth until the present, similar to other domestic animal species. Our data further suggest that a large sample of wild horse diversity was incorporated into the domestic population; specifically, at least 46 of the mtDNA lineages observed in domestic horses (73%) already existed before the beginning of domestication about 5,000 years ago.ConclusionsOur study provides a window into the maternal origins of extant domestic horses and confirms that modern domestic breeds present a wide sample of the mtDNA diversity found in ancestral, now extinct, wild horse populations. The data obtained allow us to detect a population expansion event coinciding with the beginning of domestication and to estimate both the minimum number of female horses incorporated into the domestic gene pool and the time depth of the domestic horse mtDNA gene pool.

Bayesian analysis of a morphological supermatrix sheds light on controversial fossil hominin relationships

The phylogenetic relationships of several hominin species remain controversial. Two methodological issues contribute to the uncertainty—use of partial, inconsistent datasets and reliance on phylogenetic methods that are ill-suited to testing competing hypotheses. Here, we report a study designed to overcome these issues. We first compiled a supermatrix of craniodental characters for all widely accepted hominin species. We then took advantage of recently developed Bayesian methods for building trees of serially sampled tips to test among hypotheses that have been put forward in three of the most important current debates in hominin phylogenetics—the relationship between Australopithecus sediba and Homo, the taxonomic status of the Dmanisi hominins, and the place of the so-called hobbit fossils from Flores, Indonesia, in the hominin tree. Based on our results, several published hypotheses can be statistically rejected. For example, the data do not support the claim that Dmanisi hominins and all other early Homo specimens represent a single species, nor that the hobbit fossils are the remains of small-bodied modern humans, one of whom had Down syndrome. More broadly, our study provides a new baseline dataset for future work on hominin phylogeny and illustrates the promise of Bayesian approaches for understanding hominin phylogenetic relationships.

Primary endosymbiosis events date to the later Proterozoic with cross-calibrated phylogenetic dating of duplicated ATPase proteins

Chloroplasts and mitochondria descended from bacterial ancestors, but the dating of these primary endosymbiosis events remains very uncertain, despite their importance for our understanding of the evolution of both bacteria and eukaryotes. All phylogenetic dating in the Proterozoic and before is difficult: Significant debates surround potential fossil calibration points based on the interpretation of the Precambrian microbial fossil record, and strict molecular clock methods cannot be expected to yield accurate dates over such vast timescales because of strong heterogeneity in rates. Even with more sophisticated relaxed-clock analyses, nodes that are distant from fossil calibrations will have a very high uncertainty in dating. However, endosymbiosis events and gene duplications provide some additional information that has never been exploited in dating; namely, that certain nodes on a gene tree must represent the same events, and thus must have the same or very similar dates, even if the exact date is uncertain. We devised techniques to exploit this information: cross-calibration, in which node date calibrations are reused across a phylogeny, and cross-bracing, in which node date calibrations are formally linked in a hierarchical Bayesian model. We apply these methods to proteins with ancient duplications that have remained associated and originated from plastid and mitochondrial endosymbionts: the α and β subunits of ATP synthase and its relatives, and the elongation factor thermo unstable. The methods yield reductions in dating uncertainty of 14–26% while only using date calibrations derived from phylogenetically unambiguous Phanerozoic fossils of multicellular plants and animals. Our results suggest that primary plastid endosymbiosis occurred ∼900 Mya and mitochondrial endosymbiosis occurred ∼1,200 Mya.

Genome duplication and multiple evolutionary origins of complex migratory behavior in Salmonidae

Multiple rounds of whole genome duplication have repeatedly marked the evolution of vertebrates, and correlate strongly with morphological innovation. However, less is known about the behavioral, physiological and ecological consequences of genome duplication, and whether these events coincide with major transitions in vertebrate complexity. The complex behavior of anadromy - where adult fishes migrate up rivers from the sea to their natal site to spawn - is well known in salmonid fishes. Some hypotheses suggest that migratory behavior evolved as a consequence of an ancestral genome duplication event, which permitted salinity tolerance and osmoregulatory plasticity. Here we test whether anadromy evolved multiple times within salmonids, and whether genome duplication coincided with the evolution of anadromy. We present a method that uses ancestral character simulation data to plot the frequency of character transitions over a time calibrated phylogenetic tree to provide estimates of the absolute timing of character state transitions. Furthermore, we incorporate extinct and extant taxa to improve on previous estimates of divergence times. We present the first phylogenetic evidence indicating that anadromy evolved at least twice from freshwater salmonid ancestors. Results suggest that genome duplication did not coincide in time with changes in migratory behavior, but preceded a transition to anadromy by 55-50 million years. Our study represents the first attempt to estimate the absolute timing of a complex behavioral trait in relation to a genome duplication event.