A phyloclimatic study of Cyclamen

Background

The impact of global climate change on plant distribution, speciation and extinction is of current concern. Examining species climatic preferences via bioclimatic niche modelling is a key tool to study this impact. There is an established link between bioclimatic niche models and phylogenetic diversification. A next step is to examine future distribution predictions from a phylogenetic perspective. We present such a study using Cyclamen (Myrsinaceae), a group which demonstrates morphological and phenological adaptations to its seasonal Mediterranean-type climate. How will the predicted climate change affect future distribution of this popular genus of garden plants?

Results

We demonstrate phylogenetic structure for some climatic characteristics, and show that most Cyclamen have distinct climatic niches, with the exception of several wide-ranging, geographically expansive, species. We reconstruct climate preferences for hypothetical ancestral Cyclamen. The ancestral Cyclamen lineage has a preference for the seasonal Mediterranean climate characteristic of dry summers and wet winters. Future bioclimatic niches, based on BIOCLIM and Maxent models, are examined with reference to a future climate scenario for the 2050s. Over the next 50 years we predict a northward shift in the area of climatic suitability, with many areas of current distribution becoming climatically unsuitable. The area of climatic suitability for every Cyclamen species is predicted to decrease. For many species, there may be no areas with a suitable climate regardless of dispersal ability, these species are considered to be at high risk of extinction. This risk is examined from a phylogenetic perspective.

Conclusion

Examining bioclimatic niches from a phylogenetic perspective permits novel interpretations of these models. In particular, reconstruction of ancestral niches can provide testable hypothesis about the historical development of lineages. In the future we can expect a northwards shift in climatic suitability for the genus Cyclamen. If this proves to be the case then dispersal is the best chance of survival, which seems highly unlikely for ant-dispersed Cyclamen. Human-assisted establishment of Cyclamen species well outside their native ranges offers hope and could provide the only means of dispersal to potentially suitable future environments. Even without human intervention the phylogenetic perspective demonstrates that major lineages could survive climate change even if many species are lost.     

High-resolution bioclimatic dataset derived from future climate projections for plant species distribution modeling

Species distribution modeling is playing an increasingly prominent role in ecology and global change biology, owing to its potential to predict species range shifts, biodiversity losses, and biological invasion risks for future climates. Such models are now well-established as important tools for biological conservation. However, the lack of high-resolution data for future climate scenarios has seriously limited their application, particularly because of the scale gap between general circulation models (GCMs) and species distribution models (SDMs). A recently introduced change-factor downscaling technique provides a convenient way to build high-resolution datasets from GCM projections. Here, we present a high-resolution (10’ × 10’) global bioclimatic dataset (BioPlant) for plant species distribution. The 15 bioclimatic variables we select are considered those most eco-physiologically relevant. They can be easily calculated from climatic variables common to all GCM projections. In addition to the traditional classes of variables regarding temperature and precipitation, the BioPlant dataset emphasizes the interactions between temperature and precipitation, particularly within plant growing seasons. A preliminary visual analysis shows that variations among GCMs are more significant on a species range scale than on a global scale. Thus, the formerly advocated ensemble modeling method should be applied not only to different SDMs, but also to various GCMs. Statistic analysis suggests that divergent behavior among GCM variations for temperature class variables and classes of precipitation variables requires special attention. Our dataset may provide a common platform for ensemble modeling, and can serve as an example to develop higher-resolution regional datasets.     

Adaptation, niche conservatism, and convergence: comparative studies of leaf evolution in the California chaparral

Small leaves and low specific leaf area (SLA) have long been viewed as adaptations to Mediterranean-type climates in many species of evergreen woody plants. However, paleobotanical and floristic evidence suggests that in many cases these traits originated prior to the advent of the summer-drought climate regime. In this study, molecular phylogenies and ancestral state reconstructions were used to test the hypothesis of adaptive leaf evolution in 12 lineages of evergreen shrubs in the California chaparral. Across all lineages there was a small but significant shift toward lower SLA, but there were no trends in leaf size evolution. For individual lineages, adaptive changes were detected in only three cases for SLA and in one case for leaf size. Three of these cases of evolutionary change were observed in taxa derived from cool temperate ancestors (e.g., Heteromeles). In contrast, most lineages originating from subtropical ancestors exhibited relative stasis in leaf trait evolution (e.g., Ceanothus). The absence of change suggests that ancestors of chaparral taxa had already acquired appropriate traits that contributed to their success under Mediterranean-type climates. These results illustrate how biogeographic history may influence patterns of trait evolution and adaptation and highlight the contribution of ecological sorting processes to the assembly and functional ecology of regional biotas.     

Phylogeny, historical biogeography, and patterns of diversification for Pinus (Pinaceae): phylogenetic tests of fossil-based hypotheses

Pines comprise one of the largest coniferous genera, are distributed throughout the Northern Hemisphere, and have an abundant fossil record. Distributions of fossils have been used to derive a three-step hypothesis of early pine evolution, which postulates a Mesozoic origin for the genus, east-west expansions across Laurasia, and retraction into Eocene refugia. Here, we present phylogenetic tests of this hypothesis using chloroplast sequence data from four loci for 83 pine species. We used the fossil-based hypothesis to derive null expectations concerning monophyly of taxonomic groups, dates of cladogenesis, and patterns of diversification. Phylogenetic analyses using several algorithms subsequently provided rigorous tests of these expectations. Our inferred phylogenies illustrated broad congruence with taxonomic groups, but highlighted consistent problems within subgenus Strobus. Estimated minimum dates of divergence derived from relaxed clock methods were largely consistent with the fossil record and yielded a date for the ingroup node of Pinus of 128+/-4 mya, depending upon the calibration used for subgenus Pinus. Ancestral area reconstructions showed Pinus to have most likely originated in Eurasia. Major clades differed in biogeographic patterns, but were consistent with the fossil-based hypothesis. We found weak support, however, for a change in diversification rate in the Eocene as interpretations of fossil distributions would have predicted.     

Pleistocene climate, phylogeny, and climate envelope models: an integrative approach to better understand species' response to climate change

Mean annual temperature reported by the Intergovernmental Panel on Climate Change increases at least 1.1°C to 6.4°C over the next 90 years. In context, a change in climate of 6°C is approximately the difference between the mean annual temperature of the Last Glacial Maximum (LGM) and our current warm interglacial. Species have been responding to changing climate throughout Earth's history and their previous biological responses can inform our expectations for future climate change. Here we synthesize geological evidence in the form of stable oxygen isotopes, general circulation paleoclimate models, species' evolutionary relatedness, and species' geographic distributions. We use the stable oxygen isotope record to develop a series of temporally high-resolution paleoclimate reconstructions spanning the Middle Pleistocene to Recent, which we use to map ancestral climatic envelope reconstructions for North American rattlesnakes. A simple linear interpolation between current climate and a general circulation paleoclimate model of the LGM using stable oxygen isotope ratios provides good estimates of paleoclimate at other time periods. We use geologically informed rates of change derived from these reconstructions to predict magnitudes and rates of change in species' suitable habitat over the next century. Our approach to modeling the past suitable habitat of species is general and can be adopted by others. We use multiple lines of evidence of past climate (isotopes and climate models), phylogenetic topology (to correct the models for long-term changes in the suitable habitat of a species), and the fossil record, however sparse, to cross check the models. Our models indicate the annual rate of displacement in a clade of rattlesnakes over the next century will be 2 to 3 orders of magnitude greater (430-2,420 m/yr) than it has been on average for the past 320 ky (2.3 m/yr).     

Molecular evidence for the common origin of snap-traps among carnivorous plants

The snap-trap leaves of the aquatic waterwheel plant (Aldrovanda) resemble those of Venus' flytrap (Dionaea), its distribution and habit are reminiscent of bladderworts (Utricularia), but it shares many reproductive characters with sundews (Drosera). Moreover, Aldrovanda has never been included in molecular phylogenetic studies, so it has been unclear whether snap-traps evolved only once or more than once among angiosperms. Using sequences from nuclear 18S and plastid rbcL, atpB, and matK genes, we show that Aldrovanda is sister to Dionaea, and this pair is sister to Drosera. Our results indicate that snap-traps are derived from flypaper-traps and have a common ancestry among flowering plants, despite the fact that this mechanism is used by both a terrestrial species and an aquatic one. Genetic and fossil evidence for the close relationship between these unique and threatened organisms indicate that carnivory evolved from a common ancestor within this caryophyllid clade at least 65 million years ago.     

The evolutionary relations of sunken, covered, and encrypted stomata to dry habitats in Proteaceae

Sunken, covered, and encrypted stomata have been anecdotally linked with dry climates and reduced transpiration and therefore have been used to infer dry palaeoclimates from fossils. This study assesses the evolutionary and ecological associations of such stomatal protection in a model system-the diverse southern hemisphere family Proteaceae. Analyses were based on the morphology of over 1400 Australian, South African, New Caledonian, New Zealand, and South American species, anatomy of over 300 of these species, and bioclimatic data from all 1109 Australian species. Ancestral state reconstruction revealed that five or six evolutionary transitions explain over 98% of the dry climate species in the family, with a few other, minor invasions of dry climates. Deep encryption, i.e., stomata in deep pits, in grooves, enclosed by tightly revolute margins or strongly overarched by cuticle, evolved at least 11 times in very dry environments. Other forms of stomatal protection (sunken but not closely encrypted stomata, papillae, and layers of hairs covering the stomata) also evolved repeatedly, but had no systematic association with dry climates. These data are evidence for a strong distinction in function, with deep encryption being an adaptation to aridity, whereas broad pits and covered stomata have more complex relations to climate.     

The uneven phylogeny and biogeography of Erodium (Geraniaceae): radiations in the Mediterranean and recent recurrent intercontinental colonization

Background and Aims

The genus Erodium is a common feature of Mediterranean-type climates throughout the world, but the Mediterranean Basin has significantly higher diversity than other areas. The aim here is to reveal the biogeographical history of the genus and the causes behind the evolution of the uneven distribution.

Methods

Seventy-eight new nrITS sequences were incorporated with existing plastid data to explore the phylogenetic relationships and biogeography of Erodium using several reconstruction methods. Divergence times for major clades were calculated and contrasted with other previously published information. Furthermore, topological and temporal diversification rate shift analyses were employed using these data.

Key Results

Phylogenetic relationships among species are widely congruent with previous plastid reconstructions, which refute the classical taxonomical classification. Biogeographical reconstructions point to Asia as the ancestral area of Erodium, arising approx. 18 MYA. Four incidences of intercontinental dispersal from the Mediterranean Basin to similar climates are demonstrated. Increases in diversification were present in two independent Erodium lineages concurrently. Two bursts of diversification (3 MYA and 0·69 MYA) were detected only in the Mediterranean flora.

Conclusions

Two lineages diverged early in the evolution of the genus Erodium: (1) subgenus Erodium plus subgenus Barbata subsection Absinthioidea and (2) the remainder of subgenus Barbata. Dispersal across major water bodies, although uncommon, has had a major influence on the distribution of this genus and is likely to have played as significant role as in other, more easily dispersed, genera. Establishment of Mediterranean climates has facilitated the spread of the genus and been crucial in its diversification. Two, independent, rapid radiations in response to the onset of drought and glacial climate change indicate putative adaptive radiations in the genus.     

A closer look at novel climates: new methods and insights at continental to landscape scales

Novel climates – emerging conditions with no analog in the observational record – are an open problem in ecological modeling. Detecting extrapolation into novel conditions is a critical step in evaluating bioclimatic projections of how species and ecosystems will respond to climate change. However, biologically informed novelty detection methods remain elusive for many modeling algorithms. To assist with bioclimatic model design and evaluation, we present a first‐approximation assessment of general novelty based on a simple and consistent characterization of climate. We build on the seminal global analysis of Williams et al. (2007 PNAS, 104, 5738) by assessing of end‐of‐21st‐century novelty for North America at high spatial resolution and by refining their standardized Euclidean distance into an intuitive Mahalanobian metric called sigma dissimilarity. Like this previous study, we found extensive novelty in end‐of‐21st‐century projections for the warm southern margin of the continent as well as the western Arctic. In addition, we detected localized novelty in lower topographic positions at all latitudes: By the end of the 21st century, novel climates are projected to emerge at low elevations in 80% and 99% of ecoregions in the RCP4.5 and RCP8.5 emissions scenarios, respectively. Novel climates are limited to 7% of the continent's area in RCP4.5, but are much more extensive in RCP8.5 (40% of area). These three risk factors for novel climates – regional susceptibility, topographic position, and the magnitude of projected climate change – represent a priori evaluation criteria for the credibility of bioclimatic projections. Our findings indicate that novel climates can emerge in any landscape. Interpreting climatic novelty in the context of nonlinear biological responses to climate is an important challenge for future research.     

The impact of climate change on the distribution of two threatened Dipterocarp trees

Two ecologically and economically important, and threatened Dipterocarp trees Sal (Shorea robusta) and Garjan (Dipterocarpus turbinatus) form mono‐specific canopies in dry deciduous, moist deciduous, evergreen, and semievergreen forests across South Asia and continental parts of Southeast Asia. They provide valuable timber and play an important role in the economy of many Asian countries. However, both Dipterocarp trees are threatened by continuing forest clearing, habitat alteration, and global climate change. While climatic regimes in the Asian tropics are changing, research on climate change‐driven shifts in the distribution of tropical Asian trees is limited. We applied a bioclimatic modeling approach to these two Dipterocarp trees Sal and Garjan. We used presence‐only records for the tree species, five bioclimatic variables, and selected two climatic scenarios (RCP4.5: an optimistic scenario and RCP8.5: a pessimistic scenario) and three global climate models (GCMs) to encompass the full range of variation in the models. We modeled climate space suitability for both species, projected to 2070, using a climate envelope modeling tool “MaxEnt” (the maximum entropy algorithm). Annual precipitation was the key bioclimatic variable in all GCMs for explaining the current and future distributions of Sal and Garjan (Sal: 49.97 ± 1.33; Garjan: 37.63 ± 1.19). Our models predict that suitable climate space for Sal will decline by 24% and 34% (the mean of the three GCMs) by 2070 under RCP4.5 and RCP8.5, respectively. In contrast, the consequences of imminent climate change appear less severe for Garjan, with a decline of 17% and 27% under RCP4.5 and RCP8.5, respectively. The findings of this study can be used to set conservation guidelines for Sal and Garjan by identifying vulnerable habitats in the region. In addition, the natural habitats of Sal and Garjan can be categorized as low to high risk under changing climates where artificial regeneration should be undertaken for forest restoration.     

Tropical niche conservatism as a historical narrative hypothesis for the Neotropics: a case study using the fly family Muscidae

Aim We evaluate the extent to which the tropical conservatism hypothesis can explain the evolutionary development of the Muscidae. Furthermore, we compare the geographical patterns of muscid phylogenetic structure with biogeographical regions that have been identified for Neotropical insects. Location Central and South America. Methods We modelled the geographic distributions of 658 species using Maxent and 19 environmental variables. A generic‐level supertree of the Muscidae was assembled using matrix representation with parsimony and used to map the geographic pattern of mean root distance (MRD), a metric of the relative evolutionary development of assemblages. Regression models (ordinary least squares and regression trees) were used to examine temperature and other environmental correlates of MRD to explore potential environmental drivers of muscid diversification. We used the regression tree results to recognize variable intervals that best explained MRD, and these intervals were mapped to recognize and compare with biogeographical regions of Neotropical insects. Results The geographic pattern of MRD was consistent with the tropical conservatism hypothesis: species in genera that diversified relatively early, as measured by their distance from the tree root, dominate lowland tropical South America, whereas species in genera that diversified more recently occupy extra‐tropical areas, sub‐Antarctic areas and the Andean highlands. Temperature was the strongest correlate of MRD. Three biogeographical regions were recognized and they coincided with two regions known for insects. Main conclusions Evolutionary responses of muscid flies to post‐Eocene climate change taking the form of an expansion of a tropical group into regions with colder climates may be fundamental to explaining their distribution in the Neotropics. Our biogeographical regions delimited by temperature and the phylogenetic metric, surrogates of the tropical conservatism hypothesis, were very similar to general insect patterns, supporting the ‘tropical origin and evolutionary response to climate cooling’ as a broadly based historical narrative for the Neotropics.     

Droseraceae germination patterns and their taxonomic significance

The Droseraceae exhibit a range of"germination patterns which are of possible taxonomic usefulness at the sectional and higher levels. Three patterns were observed in the family: phanerocotylar ( Drosera subgen. Drosera and Regia ); cryptocotylar (subgen. Ergaleium and Rorella ); and a new category, hemi-cryptocotylar, where both cotyledon apices remain in the seed coat, but the remainder emerges forming a photosynthetic cotyledon loop ( Dionaea, Drosophyllum and Drosera adelae ). Subgenus Drosera , especially sect. Drosera , is heterogenous for germination, and other features, with Drosera indica , sect. Lasiocephala and D. neocaledonica anomalous on current placements, and in need of further study. Conversely, the merger of sects Psycophila and Stelogyne and subgenl Ptycnostigma with subgen. Drosera sect. Drosera is supported by their germination features. Further studies are needed to determine the significance of environmental effects on the germination characteristics, although because the results of this study largely agree with recent morphological and molecular studies, this suggests that germination characteristics are useful at the sectional level, potentially providing additional characters for phylogenetic investigations within the Droseraceae.     

Stem architecture in Eleocharis subgenus Limnochloa (Cyperaceae): Evidence of dynamic morphological evolution in a group of pantropical sedges

We examined phylogenetic relationships and patterns of stem structural evolution in Eleocharis subgenus Limnochloa, an ecologically and economically important group of tropical to temperate-growing sedges, whose stems serve as the primary photosynthetic organs. We used maximum parsimony, likelihood, and Bayesian inference to develop phylogenetic trees and stochastic mapping and a Markov one-rate model to develop character history reconstructions of stem architecture. A complex history of stem shape evolution characterized by a high degree of homoplasy and rapid rates of change (an average of 13 transitions per character history for about 25 species) was identified across subgenus Limnochloa. Character states transition much more frequently in some lineages than others, but tend to follow a consistent directional pattern of evolutionary change. Our data also suggest that changes in stem shape and anatomy may be associated with speciation events in the subgenus (Pagel's κ = 0.3503, P = 0.04579) and may have some adaptive significance. The potential adaptive roles of stem structural traits are unclear, but may be elucidated by further studies. This work serves as a starting point for future evolutionary studies of stem shape and structure in monocots and provides important background knowledge for further studies of ecological adaptations of Eleocharis.     

A comprehensive phylogeography of the widespread pond snail genus Radix revealed restricted colonization due to niche conservatism

To clarify the effect of niche conservatism on evolutionary history, we focused on freshwater snails, which have different ecological and phylogenetic properties from previously tested taxa. We conducted a phylogenetic analysis using 750 lymnaeid individuals from 357 sites of eleven Radix species. Then, we estimated the ancestral distribution using the geographic coordinates and colonization routes. In addition, a statistical test of the colonization distances in the latitudinal and longitudinal directions was performed. We also conducted ecological niche modeling for two widely distributed species using climatic data. Ancestral geographic reconstruction estimated the origin of the genus to be around the Indian subcontinental region and showed that latitudinal immigration distances were shorter than longitudinal immigration distances in the diversification process. Ecological niche models suggested that the current distribution was restricted by climate, with annual mean temperature and precipitation of the driest month as particularly strong factors. Niche conservatism to the climate can affect the diversification of freshwater snails.     

Defining and characterizing high-rainfall Mediterranean climates

Abstract

The world's five Mediterranean-climate regions are typified by similarities in climate reflected in structural vegetation patterns. We developed a methodology to define high-rainfall (annual precipitation ≥800 mm) Mediterranean climates and contrast patterns of between- and within-region climatic heterogeneity. Climatic indices describing the seasonality of the climate were computed in Geographic Information Systems and included in a numerical analysis, in addition to selected bioclimatic variables, using the pattern analysis program PATN. Selected locations from high-rainfall Mediterranean-climate regions were grouped according to climatic similarity, and within-region climatic heterogeneity was compared between regions. Areas traditionally not considered as Mediterranean-climate regions emerged in the classification. Only the Mediterranean-type systems within the Pacific north-west of North America and south-central Chile comprised a substantial extent of high-rainfall Mediterranean climate. Both of these regions were characterized by a high climatic diversity and steep topographic gradients. The numerical analysis demonstrated the high diversity of the high-rainfall Mediterranean-climate type and differences in within-region climatic heterogeneity between the world's high-rainfall Mediterranean-climate regions.     

The future of cold‐adapted plants in changing climates: Micranthes (Saxifragaceae) as a case study

Research has shown species undergoing range contractions and/or northward and higher elevational movements as a result of changing climates. Here, we evaluate how the distribution of a group of cold‐adapted plant species with similar evolutionary histories changes in response to warming climates. We selected 29 species of Micranthes (Saxifragaceae) representing the mountain and Arctic biomes of the Northern Hemisphere. For this analysis, 24,755 data points were input into ecological niche models to assess both present fundamental niches and predicted future ranges under climate change scenarios. Comparisons were made across the Northern Hemisphere between all cold‐adapted Micranthes, including Arctic species, montane species, and species defined as narrow endemics. Under future climate change models, 72% of the species would occupy smaller geographical areas than at present. This loss of habitat is most pronounced in Arctic species in general, but is also prevalent in species restricted to higher elevations in mountains. Additionally, narrowly endemic species restricted to high elevations were more susceptible to habitat loss than those species found at lower elevations. Using a large dataset and modeling habitat suitability at a global scale, our results empirically model the threats to cold‐adapted species as a result of warming climates. Although Arctic and alpine biomes share many underlying climate similarities, such as cold and short growing seasons, our results confirm that species in these climates have varied responses to climate change and that key abiotic variables differ between these two habitats.     

Evolutionary model of protein secondary structure capable of revealing new biological relationships

Ancestral sequence reconstruction has had recent success in decoding the origins and the determinants of complex protein functions. However, phylogenetic analyses of remote homologues must handle extreme amino acid sequence diversity resulting from extended periods of evolutionary change. We exploited the wealth of protein structures to develop an evolutionary model based on protein secondary structure. The approach follows the differences between discrete secondary structure states observed in modern proteins and those hypothesized in their immediate ancestors. We implemented maximum likelihood-based phylogenetic inference to reconstruct ancestral secondary structure. The predictive accuracy from the use of the evolutionary model surpasses that of comparative modeling and sequence-based prediction; the reconstruction extracts information not available from modern structures or the ancestral sequences alone. Based on a phylogenetic analysis of a sequence-diverse protein family, we showed that the model can highlight relationships that are evolutionarily rooted in structure and not evident in amino acid-based analysis.     

Climate change effects on animal and plant phylogenetic diversity in southern Africa

Much attention has been paid to the effects of climate change on species' range reductions and extinctions. There is however surprisingly little information on how climate change driven threat may impact the tree of life and result in loss of phylogenetic diversity (PD). Some plant families and mammalian orders reveal nonrandom extinction patterns, but many other plant families do not. Do these discrepancies reflect different speciation histories and does climate induced extinction result in the same discrepancies among different groups? Answers to these questions require representative taxon sampling. Here, we combine phylogenetic analyses, species distribution modeling, and climate change projections on two of the largest plant families in the Cape Floristic Region (Proteaceae and Restionaceae), as well as the second most diverse mammalian order in Southern Africa (Chiroptera), and an herbivorous insect genus (Platypleura) in the family Cicadidae to answer this question. We model current and future species distributions to assess species threat levels over the next 70 years, and then compare projected with random PD survival. Results for these animal and plant clades reveal congruence. PD losses are not significantly higher under predicted extinction than under random extinction simulations. So far the evidence suggests that focusing resources on climate threatened species alone may not result in disproportionate benefits for the preservation of evolutionary history.     

A climate for speciation: rapid spatial diversification within the Sorex cinereus complex of shrews

The cyclic climate regime of the late Quaternary caused dramatic environmental change at high latitudes. Although these events may have been brief in periodicity from an evolutionary standpoint, multiple episodes of allopatry and divergence have been implicated in rapid radiations of a number of organisms. Shrews of the Sorex cinereus complex have long challenged taxonomists due to similar morphology and parapatric geographic ranges. Here, multi-locus phylogenetic and demographic assessments using a coalescent framework were combined to investigate spatiotemporal evolution of 13 nominal species with a widespread distribution throughout North America and across Beringia into Siberia. For these species, we first test a hypothesis of recent differentiation in response to Pleistocene climate versus more ancient divergence that would coincide with pre-Pleistocene perturbations. We then investigate the processes driving diversification over multiple continents. Our genetic analyses highlight novel diversity within these morphologically conserved mammals and clarify relationships between geographic distribution and evolutionary history. Demography within and among species indicates both regional stability and rapid expansion. Ancestral ecological differentiation coincident with early cladogenesis within the complex enabled alternating and repeated episodes of allopatry and expansion where successive glacial and interglacial phases each promoted divergence. The Sorex cinereus complex constitutes a valuable model for future comparative assessments of evolution in response to cyclic environmental change.     

Codiversification in an ant-plant mutualism: stem texture and the evolution of host use in Crematogaster (Formicidae: Myrmicinae) inhabitants of Macaranga (Euphorbiaceae)

We investigate the evolution of host association in a cryptic complex of mutualistic Crematogaster (Decacrema) ants that inhabits and defends Macaranga trees in Southeast Asia. Previous phylogenetic studies based on limited samplings of Decacrema present conflicting reconstructions of the evolutionary history of the association, inferring both cospeciation and the predominance of host shifts. We use cytochrome oxidase I (COI) to reconstruct phylogenetic relationships in a comprehensive sampling of the Decacrema inhabitants of Macaranga. Using a published Macaranga phylogeny, we test whether the ants and plants have cospeciated. The COI phylogeny reveals 10 well-supported lineages and an absence of cospeciation. Host shifts, however, have been constrained by stem traits that are themselves correlated with Macaranga phylogeny. Earlier lineages of Decacrema exclusively inhabit waxy stems, a basal state in the Pachystemon clade within Macaranga, whereas younger species of Pachystemon, characterized by nonwaxy stems, are inhabited only by younger lineages of Decacrema. Despite the absence of cospeciation, the correlated succession of stem texture in both phylogenies suggests that Decacrema and Pachystemon have diversified in association, or codiversified. Subsequent to the colonization of the Pachystemon clade, Decacrema expanded onto a second clade within Macaranga, inducing the development of myrmecophytism in the Pruinosae group. Confinement to the aseasonal wet climate zone of western Malesia suggests myrmecophytic Macaranga are no older than the wet forest community in Southeast Asia, estimated to be about 20 million years old (early Miocene). Our calculation of COI divergence rates from several published arthropod studies that relied on tenable calibrations indicates a generally conserved rate of approximately 1.5% per million years. Applying this rate to a rate-smoothed Bayesian chronogram of the ants, the Decacrema from Macaranga are inferred to be at least 12 million years old (mid-Miocene). However, using the extremes of rate variation in COI produces an age as recent as 6 million years. Our inferred timeline based on 1.5% per million years concurs with independent biogeographical events in the region reconstructed from palynological data, thus suggesting that the evolutionary histories of Decacrema and their Pachystemon hosts have been contemporaneous since the mid-Miocene. The evolution of myrmecophytism enabled Macaranga to radiate into enemy-free space, while the ants' diversification has been shaped by stem traits, host specialization, and geographic factors. We discuss the possibility that the ancient and exclusive association between Decacrema and Macaranga was facilitated by an impoverished diversity of myrmecophytes and phytoecious (obligately plant inhabiting) ants in the region.