Juan L. Cantalapiedra

Dietary innovations spurred the diversification of ruminants during the Caenozoic

Global climate shifts and ecological flexibility are two major factors that may affect rates of speciation and extinction across clades. Here, we connect past climate to changes in diet and diversification dynamics of ruminant mammals. Using novel versions of Multi-State Speciation and Extinction models, we explore the most likely scenarios for evolutionary transitions among diets in this clade and ask whether ruminant lineages with different feeding styles (browsing, grazing and mixed feeding) underwent differential rates of diversification concomitant with global temperature change. The best model of trait change had transitions from browsers to grazers via mixed feeding, with appreciable rates of transition to and from grazing and mixed feeding. Diversification rates in mixed-feeder and grazer lineages tracked the palaeotemperature curve, exhibiting higher rates during the Miocene thermal maxima. The origination of facultative mixed diet and grazing states may have triggered two adaptive radiations—one during the Oligocene–Miocene transition and the other during Middle-to-Late Miocene. Our estimate of mixed diets for basal lineages of both bovids and cervids is congruent with fossil evidence, while the reconstruction of browser ancestors for some impoverished clades—Giraffidae and Tragulidae—is not. Our results offer model-based neontological support to previous palaeontological findings and fossil-based hypothesis highlighting the importance of dietary innovations—especially mixed feeding—in the success of ruminants during the Neogene.

Biomic specialization and speciation rates in ruminants (Cetartiodactyla, Mammalia): a test of the resource-use hypothesis at the global scale.

The resource-use hypothesis proposed by E.S. Vrba predicts that specialist species have higher speciation and extinction rates than generalists because they are more susceptible to environmental changes and vicariance. In this work, we test some of the predictions derived from this hypothesis on the 197 extant and recently extinct species of Ruminantia (Cetartiodactyla, Mammalia) using the biomic specialization index (BSI) of each species, which is based on its distribution within different biomes. We ran 10000 Monte Carlo simulations of our data in order to get a null distribution of BSI values against which to contrast the observed data. Additionally, we drew on a supertree of the ruminants and a phylogenetic likelihood-based method (QuaSSE) for testing whether the degree of biomic specialization affects speciation rates in ruminant lineages. Our results are consistent with the predictions of the resource-use hypothesis, which foretells a higher speciation rate of lineages restricted to a single biome (BSI = 1) and higher frequency of specialist species in biomes that underwent high degree of contraction and fragmentation during climatic cycles. Bovids and deer present differential specialization across biomes; cervids show higher specialization in biomes with a marked hydric seasonality (tropical deciduous woodlands and schlerophyllous woodlands), while bovids present higher specialization in a greater variety of biomes. This might be the result of divergent physiological constraints as well as a different biogeographic and evolutionary history.

Decoupled ecomorphological evolution and diversification in Neogene-Quaternary horses

What drives divergence? Horse evolution has long been held as a classic example of adaptive radiation. It has been thought that an increase in the height of cheek teeth opened up new grass resources, leading to divergence. Cantalapiedra et al., however, found that although the Equinae have experienced high levels of divergence, these splits do not appear to have been related initially to specific phenotypic changes. Instead, it seems that external environmental drivers and patterns of migration and isolation initiated population divergence, with phenotypic changes emerging once lineages had begun to divide. Science, this issue p. 627 Diversification of horse lineages was controlled mainly by ecological limits rather than rapid phenotypic changes Evolutionary theory has long proposed a connection between trait evolution and diversification rates. In this work, we used phylogenetic methods to evaluate the relationship of lineage-specific speciation rates and the mode of evolution of body size and tooth morphology in the Neogene and Quaternary radiation of horses (7 living and 131 extinct species). We show that diversification pulses are a recurrent feature of equid evolution but that these pulses are not correlated with rapid bursts in phenotypic evolution. Instead, rapid cladogenesis seems repeatedly associated with extrinsic factors that relaxed diversity bounds, such as increasing productivity and geographic dispersals into the Old World. This evidence suggests that diversity dynamics in Equinae were controlled mainly by ecological limits under diversity dependence rather than rapid ecomorphological differentiation.

Global climate changes drive ecological specialization of mammal faunas: trends in rodent assemblages from the Iberian Plio-Pleistocene

BackgroundSeveral macroevolutionary hypotheses propose a synchrony between climatic changes and variations in the structure of faunal communities. Some of them focus on the importance of the species ecological specialization because of its effects on evolutionary processes and the resultant patterns. Particularly, Vrba’s turnover pulse hypothesis and resource-use hypothesis revolve around the importance of biome inhabitation. In order to test these hypotheses, we used the Biomic Specialization Index, which is based on the number of biomes occupied by each species, and evaluated the changes in the relative importance of generalist and specialist rodents in more than forty fossil sites from the Iberian Plio-Pleistocene.ResultsOur results indicate that there was a decrease in the specialization degree of rodent faunas during the Pliocene due to the global cooling that triggered the onset of the glacial events of the Cenozoic (around 2.75 Ma). The subsequent faunal transition after this critical paleoenvironmental event was characterized by an increase of specialization related to the adaptation to the new environmental conditions, which was mainly associated with the Pleistocene radiation of Arvicolinae (voles).ConclusionsThe pattern of faunal turnover is correlated with the development of the modern glaciations in the Northern Hemisphere around 2.75 Ma, and represents a reorganization of the rodent communities, as suggested by the turnover pulse hypothesis. Our data also support the resource-use hypothesis, which presumes the role of the degree of specialization in resources specifically related to particular biomes as a driver of differential speciation and extinction rates. These results stress the intimate connection between ecological and evolutionary changes.

A macroecological glance at the structure of late Miocene rodent assemblages from Southwest Europe

Deep-time perspectives in macroecology are essential with regard to understanding the impact of climate forcing on faunal communities. Using late Miocene rodent faunas (12 to 5 Ma) from two different biogeographical provinces from southwestern Europe, we asked whether the waxing and waning of faunas with dissimilar ecological affinities tracked climate in different ways. The latest middle Miocene featured a fauna dominated by dormice with forest and mixed-habitat affinities. This group declined towards the Upper Miocene. Rodent taxa with the highest values of richness at the beginning of the Upper Miocene are generalists in the southern province and specialists of forested habitats in the northern province. Finally, we identified a third, increasingly significant group of rodents linked to open landscapes towards the end of the Miocene. These three broad ecological groups showed differential responses to a complex set of interconnected circumstances, including the biogeographic structure of the study area and climatic changes throughout time.

Systematics and evolution of the Miocene three-horned palaeomerycid ruminants (Mammalia, Cetartiodactyla)

Palaeomerycids were strange three-horned Eurasian Miocene ruminants known through fossils from Spain to China. We here study their systematics, offering the first cladistic phylogeny of the best-known species of the group, and also reassess their phylogenetic position among ruminants, which is currently disputed. The beautifully preserved remains of a new palaeomerycid from middle Miocene deposits of Spain, Xenokeryx amidalae gen. et sp. nov., helps us to better understand palaeomerycid anatomy, especially that of the nuchal region in the skull, significantly improving our current knowledge on these enigmatic ruminants. Our results show two main lineages of palaeomerycids, one containing the genus Ampelomeryx diagnosed by a characteristic type of cranium / cranial appendages and some dental derived traits, and another one that clusters those forms more closely related to Triceromeryx than to Ampelomeryx, characterized by a more derived dentition and a set of apomorphic cranial features. Xenokeryx branches as a basal offshoot of this clade. Also, we find that Eurasian palaeomerycids are not closely related to North American dromomerycids, thus rejecting the currently more accepted view of palaeomerycids as the Eurasian part of the dromomerycid lineage. Instead of this, palaeomerycids are nested with the African Miocene pecoran Propalaeoryx and with giraffoids. On the other hand, dromomerycids are closely related to cervids. We define a clade Giraffomorpha that includes palaeomerycids and giraffids, and propose an emended diagnosis of the Palaeomerycidae based on cranial and postcranial characters, including several features of the cranium not described so far. We also define the Palaeomerycidae as the least inclusive clade of pecorans containing Triceromeryx and Ampelomeryx. Finally, we reassess the taxonomy of several palaeomerycid taxa.

Congruent phylogenetic and fossil signatures of mammalian diversification dynamics driven by Tertiary abiotic change.

Computational methods for estimating diversification rates from extant species phylogenetic trees have become abundant in evolutionary research. However, little evidence exists about how their outcome compares to a complementary and direct source of information: the fossil record. Furthermore, there is virtually no direct test for the congruence of evolutionary rates based on these two sources. This task is only achievable in clades with both a well‐known fossil record and a complete phylogenetic tree. Here, we compare the evolutionary rates of ruminant mammals as estimated from their vast paleontological record—over 1200 species spanning 50 myr—and their living‐species phylogeny. Significantly, our results revealed that the ruminants fossil record and phylogeny reflect congruent evolutionary processes. The concordance is especially strong for the last 25 myr, when living groups became a dominant part of ruminant diversity. We found empirical support for previous hypotheses based on simulations and neontological data: The pattern captured by the tree depends on how clade specific the processes are and which clades are involved. Also, we report fossil evidence for a postradiation speciation slowdown coupled with constant, moderate extinction in the Miocene. The recent deceleration in phylogenetic rates is connected to rapid extinction triggered by recent climatic fluctuations.

Ecological correlates of ghost lineages in ruminants

Abstract Integration between phylogenetic systematics and paleontological data has proved to be an effective method for identifying periods that lack fossil evidence in the evolutionary history of clades. In this study we aim to analyze whether there is any correlation between various ecomorphological variables and the duration of these underrepresented portions of lineages, which we call ghost lineages for simplicity, in ruminants. Analyses within phylogenetic (Generalized Estimating Equations) and non-phylogenetic (ANOVAs and Pearson correlations) frameworks were performed on the whole phylogeny of this suborder of Cetartiodactyla (Mammalia). This is the first time ghost lineages are focused in this way. To test the robustness of our data, we compared the magnitude of ghost lineages among different continents and among phylogenies pruned at different ages (4, 8, 12, 16, and 20 Ma). Differences in mean ghost lineage were not significantly related to either geographic or temporal factors. Our results indicate that the proportion of the known fossil record in ruminants appears to be influenced by the preservation potential of the bone remains in different environments. Furthermore, large geographical ranges of species increase the likelihood of preservation.

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.