Evolution along allometric lines of least resistance: morphological differentiation in Pristurus geckos.

Species living in distinct habitats often experience unique ecological selective pressures, which can drive phenotypic divergence. However, how ecophenotypic patterns are affected by allometric trends and trait integration levels is less well understood. Here we evaluate the role of allometry in shaping body size and body form diversity in Pristurus geckos utilizing differing habitats. We found that patterns of allometry and integration in body form were distinct in species with different habitat preferences, with ground-dwelling Pristurus displaying the most divergent allometric trend and high levels of integration. There was also strong concordance between intraspecific allometry across individuals and evolutionary allometry among species, revealing that differences in body form among individuals were predictive of evolutionary changes across the phylogeny at macroevolutionary scales. This suggested that phenotypic evolution occurred along allometric lines of least resistance, with allometric trajectories imposing a strong influence on the magnitude and direction of size and shape changes across the phylogeny. When viewed in phylomorphospace, the largest rock-dwelling species were most similar to the smallest ground-dwelling species, and vice versa. Thus, in Pristurus, phenotypic evolution along the differing habitat-based allometric trajectories resulted in similar body forms at differing body sizes in distinct ecological habitats.

Diet versatility and functional trade-offs shape tooth morphology in squirrels.

Identifying the drivers of adaptation is key to understanding the origin and evolution of diversity. Here we study the morphological evolution of tooth morphology, a classic example of a conserved structure, to gain insights into the conditions that can overcome resistance to evolutionary change. We use geometric morphometrics of the occlusal surface outline of the fourth lower premolar (p4) of squirrels, a paradigm of a stable tooth morphology, to explore morphological adaptations to diet. Although a versatile generalist dental morphology favors the retention of the ancestral shape, the acquisition of diets that require strong mechanical processing drives morphological change. In particular, species that eat both grass and dry fruits evolved disparate tooth shape morphologies, related to trade-offs between feeding performance that lead to a more or less pronounced change depending on the proportion of those items in their diet. Also, some folivores develop relatively large p4s, and most bark gleaners have relatively small p4s. Ultimately, despite the role of diet shaping these patterns, we showed that diet is not the only factor driving the evolution of tooth morphology.

A phylogenetic study to assess the link between biome specialization and diversification in swallowtail butterflies.

The resource-use hypothesis, proposed by E.S. Vrba, states that habitat fragmentation caused by climatic oscillations would affect particularly biome specialists (species inhabiting only one biome), which might show higher speciation and extinction rates than biome generalists. If true, lineages would accumulate biome-specialist species. This effect would be particularly exacerbated for biomes located at the periphery of the global climatic conditions, namely, biomes that have high/low precipitation and high/low temperature such as rainforest (warm-humid), desert (warm-dry), steppe (cold-dry) and tundra (cold-humid). Here, we test these hypotheses in swallowtail butterflies, a clade with more than 570 species, covering all the continents but Antarctica, and all climatic conditions. Swallowtail butterflies are among the most studied insects, and they are a model group for evolutionary biology and ecology studies. Continental macroecological rules are normally tested using vertebrates, this means that there are fewer examples exploring terrestrial invertebrate patterns at global scale. Here, we compiled a large Geographic Information System database on swallowtail butterflies' distribution maps and used the most complete time-calibrated phylogeny to quantify diversification rates (DRs). In this paper, we aim to answer the following questions: (1) Are there more biome-specialist swallowtail butterflies than biome generalists? (2) Is DR related to biome specialization? (3) If so, do swallowtail butterflies inhabiting extreme biomes show higher DRs? (4) What is the effect of species distribution area? Our results showed that swallowtail family presents a great number of biome specialists which showed substantially higher DRs compared to generalists. We also found that biome specialists are unevenly distributed across biomes. Overall, our results are consistent with the resource-use hypothesis, species climatic niche and biome fragmentation as key factors promoting isolation.

Fossil biomolecules reveal an avian metabolism in the ancestral dinosaur.

Birds and mammals independently evolved the highest metabolic rates among living animals1. Their metabolism generates heat that enables active thermoregulation1, shaping the ecological niches they can occupy and their adaptability to environmental change2. The metabolic performance of birds, which exceeds that of mammals, is thought to have evolved along their stem lineage3-10. However, there is no proxy that enables the direct reconstruction of metabolic rates from fossils. Here we use in situ Raman and Fourier-transform infrared spectroscopy to quantify the in vivo accumulation of metabolic lipoxidation signals in modern and fossil amniote bones. We observe no correlation between atmospheric oxygen concentrations11 and metabolic rates. Inferred ancestral states reveal that the metabolic rates consistent with endothermy evolved independently in mammals and plesiosaurs, and are ancestral to ornithodirans, with increasing rates along the avian lineage. High metabolic rates were acquired in pterosaurs, ornithischians, sauropods and theropods well before the advent of energetically costly adaptations, such as flight in birds. Although they had higher metabolic rates ancestrally, ornithischians reduced their metabolic abilities towards ectothermy. The physiological activities of such ectotherms were dependent on environmental and behavioural thermoregulation12, in contrast to the active lifestyles of endotherms1. Giant sauropods and theropods were not gigantothermic9,10, but true endotherms. Endothermy in many Late Cretaceous taxa, in addition to crown mammals and birds, suggests that attributes other than metabolism determined their fate during the terminal Cretaceous mass extinction.

Ecological specialization, rather than the island effect, explains morphological diversification in an ancient radiation of geckos.

Island colonists are often assumed to experience higher levels of phenotypic diversification than continental taxa. However, empirical evidence has uncovered exceptions to this 'island effect'. Here, we tested this pattern using the geckos of the genus Pristurus from continental Arabia and Africa and the Socotra Archipelago. Using a recently published phylogeny and an extensive morphological dataset, we explore the differences in phenotypic evolution between Socotran and continental taxa. Moreover, we reconstructed ancestral habitat occupancy to examine if ecological specialization is correlated with morphological change, comparing phenotypic disparity and trait evolution between habitats. We found a heterogeneous outcome of island colonization. Namely, only one of the three colonization events resulted in a body size increase. However, in general, Socotran species do not present higher levels or rates of morphological diversification than continental groups. Instead, habitat specialization explains better the body size and shape evolution in Pristurus. Particularly, the colonization of ground habitats appears as the main driver of morphological change, producing the highest disparity and evolutionary rates. Additionally, arboreal species show very similar body size and head proportions. These results reveal a determinant role of ecological mechanisms in morphological evolution and corroborate the complexity of ecomorphological dynamics in continent-island systems.

Punctuated ecological equilibrium in mammal communities over evolutionary time scales.

The study of deep-time ecological dynamics has the ability to inform conservation decisions by anticipating the behavior of ecosystems millions of years into the future. Using network analysis and an exceptional fossil dataset spanning the past 21 million years, we show that mammalian ecological assemblages undergo long periods of functional stasis, notwithstanding high taxonomic volatility due to dispersal, speciation, and extinction. Higher functional richness and diversity promoted the persistence of functional faunas despite species extinction risk being indistinguishable among these different faunas. These findings, and the large mismatch between functional and taxonomic successions, indicate that although safeguarding functional diversity may or may not minimize species losses, it would certainly enhance the persistence of ecosystem functioning in the face of future disturbances.

Correction: Body-size structure of Central Iberian mammal fauna reveals semidesertic conditions during the middle Miocene Global Cooling Event.

[This corrects the article DOI: 10.1371/journal.pone.0186762.].

Differential responses of Miocene rodent metacommunities to global climatic changes were mediated by environmental context.

The study of how long-term changes affect metacommunities is a relevant topic, that involves the evaluation of connections among biological assemblages across different spatio-temporal scales, in order to fully understand links between global changes and macroevolutionary patterns. We applied multivariate statistical analyses and diversity tests using a large data matrix of rodent fossil sites in order to analyse long-term faunal changes. Late Miocene rodent faunas from southwestern Europe were classified into metacommunities, presumably sharing ecological affinities, which followed temporal and environmental non-random assembly and disassembly patterns. Metacommunity dynamics of these faunas were driven by environmental changes associated with temperature variability, but there was also some influence from the aridity shifts described for this region during the late Miocene. Additionally, while variations in the structure of rodent assemblages were directly influenced by global climatic changes in the southern province, the northern sites showed a pattern of climatic influence mediated by diversity-dependent processes.

Body-size structure of Central Iberian mammal fauna reveals semidesertic conditions during the middle Miocene Global Cooling Event.

We developed new quantitative palaeoclimatic inference models based on the body-size structure of mammal faunas from the Old World tropics and applied them to the Somosaguas fossil site (middle Miocene, central Iberian Peninsula). Twenty-six mammal species have been described at this site, including proboscideans, ungulates, carnivores, insectivores, lagomorphs and rodents. Our analyses were based on multivariate and bivariate regression models correlating climatic data and body-size structure of 63 modern mammal assemblages from Sub-Saharan Africa and the Indian subcontinent. The results showed an average temperature of the coldest month higher than 26°C for the Somosaguas fossil site, a mean annual thermal amplitude around 10°C, a drought length of 10 months, and an annual total precipitation greater than 200 mm per year, which are climate conditions typical of an ecotonal zone between the savanna and desert biomes. These results are congruent with the aridity peaks described over the middle Aragonian of Spain and particularly in the local biozone E, which includes Somosaguas. The aridity increase detected in this biozone is associated with the Middle Miocene Global Cooling Event. The environment of Somosaguas around 14 Ma was similar to the current environment in the Sahel region of North Africa, the Horn of Africa, the boundary area between the Kalahari and the Namib in Southern Africa, south-central Arabia, or eastern Pakistan and northwestern India. The distribution of modern vegetation in these regions follows a complex mosaic of plant communities, dominated by scattered xerophilous shrublands, semidesert grasslands, and vegetation linked to seasonal watercourses and ponds.

Ecomorphological characterization of murines and non-arvicoline cricetids (Rodentia) from south-western Europe since the latest Middle Miocene to the Mio-Pliocene boundary (MN 7/8-MN13).

Rodents are the most speciose group of mammals and display a great ecological diversity. Despite the greater amount of ecomorphological information compiled for extant rodent species, studies usually lack of morphological data on dentition, which has led to difficulty in directly utilizing existing ecomorphological data of extant rodents for paleoecological reconstruction because teeth are the most common or often the only micromammal fossils. Here, we infer the environmental ranges of extinct rodent genera by extracting habitat information from extant relatives and linking it to extinct taxa based on the phenogram of the cluster analysis, in which variables are derived from the principal component analysis on outline shape of the upper first molars. This phenotypic "bracketing" approach is particularly useful in the study of the fossil record of small mammals, which is mostly represented by isolated teeth. As a case study, we utilize extinct genera of murines and non-arvicoline cricetids, ranging from the Iberoccitanian latest middle Miocene to the Mio-Pliocene boundary, and compare our results thoroughly with previous paleoecological reconstructions inferred by different methods. The resultant phenogram shows a predominance of ubiquitous genera among the Miocene taxa, and the presence of a few forest specialists in the two rodent groups (Murinae and Cricetidae), along with the absence of open environment specialists in either group of rodents. This appears to be related to the absence of enduring grassland biomes in the Iberian Peninsula during the late Miocene. High consistency between our result and previous studies suggests that this phenotypic "bracketing" approach is a very useful tool.