Speciation in the fossil record

It is easy to claim that the fossil record says nothing about speciation because the biological species concept (which relies on interbreeding) cannot be applied to it and genetic studies cannot be carried out on it. However, fossilized organisms are often preserved in sufficient abundance for populations of intergrading morphs to be recognized, which, by analogy with modern populations, are probably biological species. Moreover, the fossil record is our only reliable documentation of the sequence of past events over long time intervals: the processes of speciation are generally too slow to be observed directly, and permanent reproductive isolation can only be verified with hindsight. Recent work has shown that some parts of the fossil record are astonishingly complete and well documented, and patterns of lineage splitting can be examined in detail. Marine plankton appear to show gradual speciation, with subsequent morphological differentiation of lineages taking up to 500000 years to occur. Marine invertebrates and vertebrates more commonly show punctuated patterns, with periods of rapid speciation followed by long-term stasis of species lineages.     

An exquisitely preserved harvestman (Arthropoda,Arachnida, Opiliones) from the Middle Jurassic of China

Sclerosomatids constitute the largest family of the arachnid order Opiliones, and one of the two families commonly found in the temperate regions of the northern Hemisphere. Harvestmen have a sparse fossil record in the Mesozoic, with only two species known from the Jurassic, one of them poorly preserved and none with precise phylogenetic placement. Here we report a new fossil, Mesobunus dunlopi sp. nov., from the Middle Jurassic (approx. 165 Mya) of Daohugou, Inner Mongolia, China. The new species is related to another genus of the same formation, but the preservation quality and details of the penis and pedipalps allow us to place them in the extant sclerosomatid subfamilies Gagrellinae or Leiobuninae. The first recognisable fossil in this subfamily highlights morphological stasis over ca. 165 Mya and the finding of this species along with lacustrine insects suggests a life mode similar to that of some modern sclerosomatids, and a possible connection between morphological and ecological stasis.     

Tempo does not correlate with mode in the fossil record

The dominating view of evolution based on the fossil record is that established species remain more or less unaltered during their existence. Substantial evolution is on the other hand routinely reported for contemporary populations, and most quantitative traits show high potential for evolution. These contrasting observations on long‐ and short‐time scales are often referred to as the paradox of stasis, which rests on the fundamental assumption that periods of morphological stasis in the fossil record represent minimal evolutionary change. Investigating 450 fossil time series, I demonstrate that the nonaccumulating morphological fluctuations during stasis travel similar distances in morphospace compared to lineages showing directional change. Hence, lineages showing stasis are commonly undergoing considerable amounts of evolution, but this evolution does not accumulate to produce large net evolutionary changes over time. Rates of evolutionary change across modes in the fossil record may be more homogenous than previously assumed and advocated, supporting the claim that substantial evolution is not exclusively or causally linked to the process of speciation. Instead of exemplifying minimal evolution, stasis likely represents information on the dynamics of the adaptive landscape on macroevolutionary time scales, including the persistence of adaptive zones and ecological niches over millions of years.     

Why coelacanths are not ‘living fossils’

A series of recent studies on extant coelacanths has emphasised the slow rate of molecular and morphological evolution in these species. These studies were based on the assumption that a coelacanth is a ‘living fossil’ that has shown little morphological change since the Devonian, and they proposed a causal link between low molecular evolutionary rate and morphological stasis. Here, we have examined the available molecular and morphological data and show that: (i) low intra‐specific molecular diversity does not imply low mutation rate, (ii) studies not showing low substitution rates in coelacanth are often neglected, (iii) the morphological stability of coelacanths is not supported by paleontological evidence. We recall that intra‐species levels of molecular diversity, inter‐species genome divergence rates and morphological divergence rates are under different constraints and they are not necessarily correlated. Finally, we emphasise that concepts such as ‘living fossil’, ‘basal lineage’, or ‘primitive extant species’ do not make sense from a tree‐thinking perspective. Editor's suggested further reading in BioEssays Tree thinking for all biology: the problem with reading phylogenies as ladders of progress Abstract     

Phylogenetic topology and timing of New Zealand olive shells are consistent with punctuated equilibrium

The olive shells of the genus Amalda comprises readily recognized species of marine neogastropod mollusks found around the world. The New Zealand Amalda fauna has particular notoriety as providing one of the best demonstrations of evolutionary morphological stasis, a prerequisite for punctuated equilibrium theory. An excellent fossil record includes representation of three extant endemic Amalda species used to explore patterns of form change. However, the phylogenetic relationship of the New Zealand Amalda species and the timing of their lineage splitting have not been studied, even though these would provide valuable evidence to test predictions of punctuated equilibrium. Here, we use entire mitogenome and long nuclear rRNA gene cassette data from 11 Amalda species, selected from New Zealand and around the world in light of high rates of endemicity among extant and fossil Amalda. Our inferred phylogenies do not refute the hypothesis that New Zealand Amalda are a natural monophyletic group and therefore an appropriate example of morphological stasis. Furthermore, estimates of the timing of cladogenesis from the molecular data for the New Zealand group are compatible with the fossil record for extant species and consistent with expectations of punctuated equilibrium.     

Deceleration of morphological evolution in a cryptic species complex and its link to paleontological stasis

Morphological stasis or the absence of morphological change is a well-known phenomenon in the paleontological record, yet it is poorly integrated with neontological evidence. Recent evidence suggests that cryptic species complexes may remain morphologically identical due to morphological stasis. Here, we describe a case of long-term stasis in the Stygocapitella cryptic species complex (Parergodrilidae, Orbiniida, Annelida). Using phylogenetic methods and morphological data, we find that rates of morphological evolution in Stygocapitella are significantly slower than in closely related taxa (Nerillidae, Orbiniidae). Assessment of quantitative and qualitative morphology revealed the presence of four morphotypes with only subtle differences, whereas molecular data supports 10 reproductively isolated clades. Notably, estimates for the time of Stygocapitella species divergence range from ∼275 million years to ∼18 million years, including one case of two morphologically similar species that have diverged about 140 million years ago. These findings provide evidence for morphological deceleration and long-term morphological stasis in Stygocapitella, and that speciation is not necessarily accompanied by morphological changes. The deceleration of morphological divergence in Stygocapitella can be potentially linked to niche conservatism and tracking, coupled with the fluctuating dynamics of the interstitial environment, or genetic constraints due to progenetic evolution. Finally, we conclude that failing to integrate speciation without morphological evolution in paleontology may bias estimates of rates of speciation and morphological evolution.     

DNA and Morphology Unite Two Species and 10 Million Year Old Fossils

Species definition and delimitation is a non-trivial problem in evolutionary biology that is particularly problematic for fossil organisms. This is especially true when considering the continuity of past and present species, because species defined in the fossil record are not necessarily equivalent to species defined in the living fauna. Correctly assigned fossil species are critical for sensitive downstream analysis (e.g., diversification studies and molecular-clock calibration). The marine snail genus Alcithoe exemplifies many of the problems with species identification. The paucity of objective diagnostic characters, prevalence of morphological convergence between species and considerable variability within species that are observed in Alcithoe are typical of a broad range of fossilised organisms. Using a synthesis of molecular and morphometric approaches we show that two taxa currently recognised as distinct are morphological variants of a single species. Furthermore, we validate the fossil record for one of these morphotypes by finding a concordance between the palaeontological record and divergence time of the lineage inferred using molecular-clock analysis. This work demonstrates the utility of living species represented in the fossil record as candidates for molecular-clock calibration, as the veracity of fossil species assignment can be more rigorously tested.     

A new african fossil caprin and a combined molecular and morphological bayesian phylogenetic analysis of caprini (Mammalia: Bovidae)

Given that most species that have ever existed on Earth are extinct, no evolutionary history can ever be complete without the inclusion of fossil taxa. Bovids (antelopes and relatives) are one of the most diverse clades of large mammals alive today, with over a hundred living species and hundreds of documented fossil species. With the advent of molecular phylogenetics, major advances have been made in the phylogeny of this clade; however, there has been little attempt to integrate the fossil record into the developing phylogenetic picture. We here describe a new large fossil caprin species from ca. 1.9-Ma deposits from the Middle Awash, Ethiopia. To place the new species phylogenetically, we perform a Bayesian analysis of a combined molecular (cytochrome b) and morphological (osteological) character supermatrix. We include all living species of Caprini, the new fossil species, a fossil takin from the Pliocene of Ethiopia (Budorcas churcheri), and the insular subfossil Myotragus balearicus. The combined analysis demonstrates successful incorporation of both living and fossil species within a single phylogeny based on both molecular and morphological evidence. Analysis of the combined supermatrix produces superior resolution than with either the molecular or morphological data sets considered alone. Parsimony and Bayesian analyses of the data set are also compared and shown to produce similar results. The combined phylogenetic analysis indicates that the new fossil species is nested within Capra, making it one of the earliest representatives of this clade, with implications for molecular clock calibration. Geographical optimization indicates no less than four independent dispersals into Africa by caprins since the Pliocene.     

Diverse fossil amoebae in German Mesozoic amber

Fossil amoebae are very rare, although their evolutionary history extends back into the Proterozoic. The Cenomanian amber of Schliersee (southern Germany) is very rich in micro-organisms and contains the highest diversity of fossil freshwater rhizopods (Gymnamoebia and Testacealobosia) yet discovered. Altogether seven testate amoebae and one gymnamoebian species are recorded from this Mesozoic amber. The four newly discovered taxa described in this paper can be assigned to the extant species Centropyxis delicatula , Centropyxis hirsuta , Phryganella acropodia and Phryganella paradoxa . Over 200 individuals of Phryganella paradoxa are preserved. Together with their syninclusions, the amoebae are species of limnetic or limnetic–terrestrial microcoenoses. The presence of 100-myr-old fossils with extant representatives suggests evolutionary stasis of these freshwater amoebae. However, not all modern testacean families have been recorded from Mesozoic limnetic habitats. Our experimental studies verify that naked and testate amoebae can be embedded in resins.     

The impact of fossil stratigraphic ranges on tip-calibration,and the accuracy and precision of divergence time estimates

The molecular clock provides the only viable means of establishing realistic evolutionary timescales but it remains unclear how best to calibrate divergence time analyses. Calibrations can be applied to the tips and/or to the nodes of a phylogeny. Tip-calibration is an attractive approach since it allows fossil species to be included alongside extant relatives in molecular clock analyses. However, most fossil species are known from multiple stratigraphical horizons and it remains unclear how such age ranges should be interpreted to codify tip-calibrations. We use simulations and empirical data to explore the impact on precision and accuracy of different approaches to informing tip-calibrations. In particular, we focus on the effect of using tip-calibrations defined using the oldest vs youngest stratigraphic occurrences, the full stratigraphical range, as well as confidence intervals on these data points. The results of our simulations show that using different calibration approaches leads to different divergence-time estimates and demonstrate that concentrating tip-calibrations near the root of the dated phylogeny improves both precision and accuracy of estimated divergence times. Finally, our results indicate that the highest levels of accuracy and precision are achieved when fossil tips are calibrated based on the fossil occurrence from which the morphological data were derived. These trends were corroborated by analysis of an empirical dataset for Ursidae. Overall, we conclude that tip-dating analyses should, in particular, employ tip calibrations close to the root of the tree and they should be calibrated based on the age of the fossil used to inform the morphological data used in Total Evidence Dating.     

Comparative infructescence morphology in Altingia (Altingiaceae) and discordance between morphological and molecular phylogenies

Altingia (Altingiaceae) is a tropical to subtropical Asian genus of lowland trees for which 5-15 species have been recognized. Morphological diversity, particularly of the mature infructescence, has been poorly known, especially for species with relatively localized and narrow distributions, and our understanding of Altingia has lagged behind that of its close temperate relative Liquidambar (sweet gum). In this contribution, mature infructescence structure, at the levels of anatomy, morphology, and micromorphology, and some distinctive inflorescence features, are described for five recognized species of Altingia, some for the first time. In the phylogenetic framework of both morphology and molecules, characters of Altingia contrast with those of Liquidambar and suggest that character evolution within Altingiaceae is at least partly related to geographic and climatic distribution. Differences in rates of evolution and morphological convergence suggest complex patterns of diversification in Altingiaceae at several different phylogenetic levels: (1) at the deep nodes, characters of the stem lineage fossil Microaltingia persist into crown group Altingiaceae, morphological stasis; (2) at the generic level, convergence within both Liquidambar and Altingia toward their respective habitats; (3) at the infrageneric level, morphological divergence in species diversification within Altingia, in response to diverse habitats of the eastern Asian subtropics; and (4) within the intercontinental disjunct species pair L. orientalis-L. styraciflua, morphological stasis.     

Evaluation of the fossil fish‐specific diversity in a chadian continental assemblage: Exploration of morphological continuous variation in Synodontis (Ostariophysi,Siluriformes)

In the fossil record, the quantification of continuous morphological variation has become a central issue when dealing with species identification and speciation. In this context, fossil taxa with living representatives hold great promise, because of the potential to characterise patterns of intraspecific morphological variation in extant species prior to any interpretation in the fossil record. The vast majority of catfish families fulfil this prerequisite, as most of them are represented by extant genera. However, although they constitute a major fish group in terms of distribution, and ecological and taxonomic diversity, the quantitative study of their past morphological variation has been neglected, as fossil specimens are generally identified based on the scarcest remains, that is, complete neurocrania that bear discrete characters. Consequently, a part of freshwater catfish history is unprospected and unknown. In this study, we explored the morphological continuous variation of the humeral plate shape in Synodontis catfishes using Elliptic Fourier Analysis (EFA), and compared extant members and fossil counterparts. We analysed 153 extant specimens of 11 Synodontis species present in the Chad basin, in addition to 23 fossil specimens from the Chadian fossiliferous area of Toros Menalla which is dated around 7 Ma. This highly speciose genus, which is one of the most diversified in Africa, exhibits a rich fossil record with several hundred remains mostly identified as Synodontis sp. The analysis of the outline of the humeral plate reveals that some living morphological types were already represented in the Chad Basin 7 My ago, and allows for the discovery of extinct species. Beside illuminating the complex Neogene evolutionary history of Synodontis, these results underline the interest in the ability of isolated remains to reconstruct a past dynamic history and to validate the relevance of EFA as a tool to explore specific diversity through time. J. Morphol. 277:1486–1496, 2016. © 2016 Wiley Periodicals, Inc.     

Bayesian phylogenetic estimation of fossil ages

Recent advances have allowed for both morphological fossil evidence and molecular sequences to be integrated into a single combined inference of divergence dates under the rule of Bayesian probability. In particular, the fossilized birth–death tree prior and the Lewis-Mk model of discrete morphological evolution allow for the estimation of both divergence times and phylogenetic relationships between fossil and extant taxa. We exploit this statistical framework to investigate the internal consistency of these models by producing phylogenetic estimates of the age of each fossil in turn, within two rich and well-characterized datasets of fossil and extant species (penguins and canids). We find that the estimation accuracy of fossil ages is generally high with credible intervals seldom excluding the true age and median relative error in the two datasets of 5.7% and 13.2%, respectively. The median relative standard error (RSD) was 9.2% and 7.2%, respectively, suggesting good precision, although with some outliers. In fact, in the two datasets we analyse, the phylogenetic estimate of fossil age is on average less than 2 Myr from the mid-point age of the geological strata from which it was excavated. The high level of internal consistency found in our analyses suggests that the Bayesian statistical model employed is an adequate fit for both the geological and morphological data, and provides evidence from real data that the framework used can accurately model the evolution of discrete morphological traits coded from fossil and extant taxa. We anticipate that this approach will have diverse applications beyond divergence time dating, including dating fossils that are temporally unconstrained, testing of the ‘morphological clock'', and for uncovering potential model misspecification and/or data errors when controversial phylogenetic hypotheses are obtained based on combined divergence dating analyses.This article is part of the themed issue ‘Dating species divergences using rocks and clocks’.     

Appearances can be deceptive: different diversification patterns within a group of Mediterranean earthworms (Oligochaeta, Hormogastridae)

Many recent studies on invertebrates have shown how morphology not always captures the true diversity of taxa, with cryptic speciation often being discussed in this context. Here, we show how diversification patterns can be very different in two clades of closely related earthworms in the genus Hormogaster stressing the risk of using nonspecific substitution rate values across taxa. On the one hand, the Hormogaster elisae species complex, endemic to the central Iberian Peninsula, shows morphological stasis. On the other hand, a clade of Hormogaster from the NE Iberian Peninsula shows an enormous morphological variability, with 15 described morphospecies. The H. elisae complex, however, evolves faster genetically, and this could be explained by the harsher environmental conditions to which it is confined—as detected in this study, that is, sandier and slightly poorer soils with lower pH values than those of the other species in the family. These extreme conditions could be at the same time limiting morphological evolution and thus be responsible for the observed morphological stasis in this clade. Contrarily, Hormogaster species from the NE Iberian Peninsula, although still inhabiting harsher milieu than other earthworm groups, have had the opportunity to evolve into a greater morphological disparity. An attempt to delimit species within this group following the recently proposed general mixed Yule‐coalescent method showed a higher number of entities than expected under the morphospecies concept, most probably due to the low vagility of these animals, which considerably limits gene flow between distant conspecific populations, but also because of the decoupling between morphological and genetic evolution in the H. elisae complex.     

Confrontation of morphological and molecular data: the Praomys group (Rodentia, Murinae) as a case of adaptive convergences and morphological stasis

Phylogenetic relationships in a group of 21 African rodent species designated as the Praomys group (Murinae) were investigated using morphological characters and sequence data from the complete mitochondrial cytochrome b gene and nuclear IRBP gene fragment (840bp). The molecular results confirm the monophyly of the Praomys group, including the species Malacomys verschureni, while the other Malacomys species appear very divergent. The basal relationships within the Praomys group are poorly resolved, suggesting a rapid radiation at about 7-9 million years ago based on genetic divergence rates calibrated from the fossil record. Discrepancies between molecular and morphological results probably reflect of numerous convergences as well as variations in the rates of morphological evolution among lineages. Reconstructions of the ancestral character states suggest a savannah origin for the Praomys group, along with some morphological traits conserved by stasis in savannah taxa. At the same time, forest taxa seem to be characterized by an accelerated morphological evolution, with acquisition of convergent adaptive characters.     

A morphometric analysis of extant and early miocene fossil hominoid maxillo-dental specimens

It is demonstrated in this paper that before we can hope to formulate phylogenetic relationships between and amongst fossil hominoid material it is first necessary to sex the material accurately. In order to determine whether the morphological and morphometrical variability seen in fossil specimens is due to sexual or inter species dimorphism, it is necessary to calibrate fossil specimens against extant hominoid species' morphologies. Only after fossil specimens have been sexed is it possible to differentiate between morphologies that are related to sex and those that are species specific. This will help reduce fossil misallocation. A morphometric analysis of extant and fossilProconsul hominoid material is presented. Each fossil specimen has been sexed according to symplesiomorphic sex morphologies as defined in this paper. After the fossil specimens have been sexed they are analyzed using multivariate statistics. The identification of differing sex patterns within the specimens examined here suggests that a new species ofProconsul may have to be considered.     

Habitat tracking, stasis and survival in Neogene large mammals

Species response to environmental change may vary from adaptation to the new conditions, to dispersal towards territories with better ecological settings (known as habitat tracking), and to extinction. A phylogenetically explicit analysis of habitat tracking in Caenozoic large mammals shows that species moving over longer distances during their existence survived longer. By partitioning the fossil record into equal time intervals, we showed that the longest distance was preferentially covered just before extinction. This supports the idea that habitat tracking is a key reaction to environmental change, and confirms that tracking causally prolongs species survival. Species covering longer distances also have morphologically less variable cheek teeth. Given the tight relationship between cheek teeth form and habitat selection in large mammals, this supports the well-known, yet little tested, idea that habitat tracking bolsters morphological stasis.     

Decoupling of molecular and morphological evolution in deep lineages of a meiobenthic harpacticoid copepod

Molecular and biochemical genetic analyses have revealed that many marine invertebrate taxa, including some well-studied and presumably cosmopolitan species, are actually complexes of sibling species. When morphological differences are slight and estimated divergence times are old, data suggest either unusually high rates of sequence evolution or long-term morphological stasis. Here, five gene regions (mitochondrial cytochrome oxidase subunit I and large-subunit ribosomal 16S rDNA and nuclear ITS1, 5.8S rDNA, and ITS2) were analyzed in four geographic samples of the meiobenthic harpacticoid copepod Cletocamptus deitersi. Molecular sequences revealed four extremely differentiated molecular lineages with unalignable nuclear intergenic spacers and mitochondrial uncorrected divergences reaching 25% (cytochrome oxidase) and 36% (16S rDNA). These levels of divergence are greater than those reported previously for congeneric species in diverse invertebrate taxa, including crustaceans. The nominally intraspecific divergence matches or exceeds the corresponding divergence from a known congener (Cletocamptus helobius). A molecular clock applied to the cytochrome oxidase subunit I data suggests that these lineages split in the Miocene, consistent with the fossil record of a North American Cletocamptus from the same period. Morphological differences among the major lineages are subtle but congruent with the patterns of genetic differentiation. Our conclusion, based on concordant patterns of variation in two mitochondrial and three nuclear gene regions, as well as morphological observations, is that C. deitersi in North America is composed of at least four separate species by the genealogical concordance, phylogenetic, and morphological-species criteria. Alternative explanations for the deep phylogenetic nodes and apparent morphological stasis, including high rates of sequence evolution, balancing selection, and genetic signatures of historical events, are considered unlikely.     

Eukaryotic microbes, species recognition and the geographic limits of species: examples from the kingdom Fungi

The claim that eukaryotic micro-organisms have global geographic ranges, constituting a significant departure from the situation with macro-organisms, has been supported by studies of morphological species from protistan kingdoms. Here, we examine this claim by reviewing examples from another kingdom of eukaryotic microbes, the Fungi. We show that inferred geographic range of a fungal species depends upon the method of species recognition. While some fungal species defined by morphology show global geographic ranges, when fungal species are defined by phylogenetic species recognition they are typically shown to harbour several to many endemic species. We advance two non-exclusive reasons to explain the perceived difference between the size of geographic ranges of microscopic and macroscopic eukaryotic species when morphological methods of species recognition are used. These reasons are that microbial organisms generally have fewer morphological characters, and that the rate of morphological change will be slower for organisms with less elaborate development and fewer cells. Both of these reasons result in fewer discriminatory morphological differences between recently diverged lineages. The rate of genetic change, moreover, is similar for both large and small organisms, which helps to explain why phylogenetic species of large and small organisms show a more similar distribution of geographic ranges. As a consequence of the different rates in fungi of genetic and morphological changes, genetic isolation precedes a recognizable morphological change. The final step in speciation, reproductive isolation, also follows genetic isolation and may precede morphological change.     

Species,speciation and human evolution

Human evolution is considered from the perspective of the recognition concept of species, which views species as an epiphenomenon of shared fertilisation systems in sexually reproducing organisms. It is argued that this concept predicts the controversial pattern of punctuated equilibrium, and offers an understanding of the hominid fossil evidence in line with that pattern. Changes in the nature of the fertilization system in the human lineage over time are discussed in relation to the pattern of morphological continuity between proposed species.