Parvipelvian phylogenetic relationships

We analysed the evolution of derived ichthyosaurs (Parvipelvia, Late Triassic to early Late Cretaceous) using novel data sets (Supplementary Methods, Supplementary Data 1–4). All analyses yielded topologies congruent with previous results from smaller data sets19,21, most notably the Jurassic origin of Cretaceous ichthyosaur lineages, the rapid divergence of Ophthalmosauridae into two distinct clades (Ophthalmosaurinae and Platypterygiinae) after the divergence of more basal lineages (Arthropterygius chrisorum), and the polyphyletic status of Ophthalmosaurus and Platypterygius (Fig. 1 and Supplementary Figs 1–11). For several decades, all or nearly all ichthyosaur remains from the Cretaceous have been referred to as Platypterygius20,22. The status of this taxon has been controversial23 as no phylogenetic study incorporated the type species of the genus Platypterygius platydactylus. Our equally weighted maximum parsimony analysis finds this species to be phylogenetically isolated from other species currently referred to as Platypterygius (Fig. 1 and Supplementary Figs 1 and 2). Implied weighting analysis places P. platydactylus as the sister taxon of a small clade of Albian–Cenomanian platypterygiines but all other species currently referred to as Platypterygius belong to another clade of Cretaceous platypterygiines (Supplementary Fig. 5). It is still premature to make a taxonomic decision on Platypterygius. However, the practise of assigning Cretaceous ichthyosaur remains to Platypterygius by default should be strictly avoided. The diversity dynamics of derived ichthyosaurs should be analysed at the species level rather than at genus level or above to circumvent these issues (see below).

Figure 1: Phylogeny and ecological diversity of parvipelvian ichthyosaurs. (a) Time scaled strict consensus tree arising from equal weight maximum parsimony analysis. Numbers denote >1 Bremer decay indices. Grey bars denote range extensions by specimens identified at the generic level. Colour coding of taxa refers to the results of b. (b) Cluster dendrogram based on the ecological data set, with gut-content data and the general features of each guild. (c) Teeth representative of each guild across the Late Albian–Cenomanian interval, illustrating the ecological extinction at the beginning of the Cenomanian. ‘Platypterygius campylodon’ and ‘Platypterygius’ sp. from the US are early Cenomanian in age69, Pervushovisaurus bannovkensis is Middle Cenomanian in age16 and ‘Platypterygius’ sp. from Germany is Late Cenomanian in age70. *denotes taxa from the Stoilensky/Kursk fauna. Scale bar, 50 mm. Full size image

Nodal support values within Ophthalmosauridae are smaller than those found by other analyses using smaller data sets18,19; this probably results from incorporation of numerous ophthalmosaurid taxa, many of which are based on substantially incomplete remains. However, because both phylogenetic accuracy and macroevolutionary inferences are positively impacted by increased taxon sampling24,25, and because of strong agreement on the parvipelvian tree topology between previous and present maximum parsimony analyses and Bayesian analyses, both in terms of topology and the timing of cladogenesis (see Supplementary Figs 1–12), we are confident in the adequacy of our new detailed data set and results to answer the macroevolutionary questions.

Cretaceous ichthyosaur diversity and disparity

A face-value count of observed species shows a general trend of increasing taxic richness throughout the Early Cretaceous, attaining a peak during the Late Albian (Fig. 2 and Supplementary Tables 1 and 2). Richness in the Late Albian is similar to that of well-sampled Jurassic stages20, but then declines abruptly during the Cenomanian. High diversity is apparent throughout the entire Early Cretaceous, with a marked diversity peak in between the Valanginian and Barremian interval, followed by an apparent extinction. Contrary to observed richness, the phylogenetically adjusted diversity estimates (which include counts of phylogenetic ghost lineages) suggest that ichthyosaur diversity remained high, declining only slightly through the Early Cretaceous (Fig. 2 and Supplementary Tables 3 and 4). This indicates that the apparent post-Barremian diversity loss observed in face-value species counts is an artefact of poor fossil-record sampling.

Figure 2: Ichthyosaur diversity through the Cretaceous. (a) Taxonomic/lineage richness. The orange thick line is the mean value per bin, while the light orange outline represents the range of values, encompassing all most-parsimonious trees, under both the ‘basic’ and ‘equal’ methods of branch length reconstruction (PADE, phylogeny-adjusted diversity estimate). The long-term sea-level is taken from Haq62. (b) Weighted mean observed pairwise dissimilarity compared with the Jurassic–Early Cretaceous average value. Light grey outline represents the 95% confidence interval. Bins are: Berriasian–Valanginian, Hauterivian–Barremian, Aptian, Albian, Cenomanian and Turonian. Important events and factors explaining the shape of the curve are indicated. Note the all-time disparity peak for Parvipelvia during the Hauterivian–Barremian. The average value for the Jurassic only is 0.24. (c) Sum of variances from the phylogenetically reconstructed data set, compared with the Jurassic–Early Cretaceous average values. The light orange and light grey outline represent the 95% confidence intervals. Again, an all-time disparity peak for Parvipelvia is recorded during the early Early Cretaceous. The average values for the Jurassic only are 7.53 (basic) and 9.38 (equal). (d) Ecological niches occupied per bin. *denotes data obtained from the Stoilensky/Kursk fauna. Full size image

Disparity metrics calculated from phylogenetic character distributions (weighted mean pairwise dissimilarity and sum of variances including ‘ancestors’) are congruent and have trajectories broadly matching that for phylogenetic diversity estimates (Fig. 2, Supplementary Tables 5 and 6 and Supplementary Data 4–6). Diversity and disparity metrics record high values during the Valanginian–Barremian interval, reflecting the co-occurrence of diverse platypterygiine lineages, ophthalmosaurines (Acamptonectes densus and Leninia stellans) and the archaic early parvipelvian Malawania anachronus. Although phylogenetic characters contain a strong signal related to phylogenetic distance26, we note that these taxa also show divergent skeletal architecture (Supplementary Figs 13–15), consistent with the observation of high disparity. Surprisingly, the Valanginian–Barremian interval records the highest disparity values for the entire history of Parvipelvia, with much higher values than the average for the entire Jurassic–Early Cretaceous interval (Fig. 2). Early Jurassic parvipelvians are not sampled at the species level, but all genera are represented in the data set (Supplementary Tables 1 and 2; Supplementary Methods); we do not anticipate that the inclusion of additional Early Jurassic species would substantially alter these results.

Disparity is decoupled from taxic/phylogenetic diversity from the Aptian onwards, declining steadily to values well below the Jurassic–Early Cretaceous average (Fig. 2). Nevertheless, it is possible that late Aptian–Albian disparity was higher than estimated here, because no ophthalmosaurine (youngest record at the Albian–Cenomanian boundary18) from that interval could be coded into the phylogenetic data set; disparity values for those bins thus only rely on platypterygiines. This disparity decrease may therefore have occurred later and more abruptly than suggested by our estimates (Fig. 2). After the earliest Cenomanian, ichthyosaurs were clearly reduced to a very limited range of morphologies with low disparity (Supplementary Figs 13–15).

Evolutionary and extinction rates

Most of the phylogenetic diversity of parvipelvians evolved during the Late Triassic–Middle Jurassic interval (Fig. 3) and not during the Cretaceous, consistent with the results of other recent studies19,27. Peaks of cladogenesis are recorded during the Late Triassic, giving rise to the ‘Neoichthyosaurian Radiation’19 (Figs 1 and 3 and Supplementary Tables 7–9). The ‘Ophthalmosaurid Radiation’ occurs as a series of peaks spanning the Early–Middle Jurassic. We also recover a platypterygiine radiation during the Berriasian–Hauterivian stages of the Early Cretaceous. This radiation is a modest relative to those of the Triassic and Jurassic; it nevertheless, gave rise to the taxa that dominated the ichthyosaur faunas of the mid-Cretaceous and up to their final extinction in the early Late Cretaceous. Rapid rates of morphological evolution based on phenotypic characters are concentrated along the lineages connecting early ichthyosaurs to Platypterygiinae, but zero branches have rapid rates of phenotypic evolution within either Ophthalmosaurinae or Platypterygiinae (Fig. 3 and Supplementary Table 9), indicating that Cretaceous ichthyosaurs had slow rates of phenotypic evolution. Furthermore, mean rates of phenotypic evolution decelerated earlier than rates of cladogenesis, becoming low from the Early Jurassic onwards (Fig. 3). Therefore, low rates of morphological evolution coincided with low-to-null rates of cladogenesis during the Cretaceous, in a combination not seen in earlier intervals. Absolute extinction rates are elevated during the Cretaceous but the estimated per-lineage extinction rates of the Early Cretaceous are generally lower than those of the Triassic and the Jurassic. Per-lineage extinction rates are elevated at the beginning and throughout the Cenomanian (Fig. 4 and Supplementary Tables 10 and 11).

Figure 3: Evolution and extinction rates for parvipelvian ichthyosaurs. (a) Median rate of morphological evolution (morphological clock) arising from the constrained Bayesian inference. (b) Median rate of morphological evolution (morphological clock) arising from the unconstrained Bayesian inference. Both analyses indicate high rates in the early evolution of Parvipelvia, confined in the Triassic (c). (d) Cladogenesis rate using the time scaled trees arising from the constrained Bayesian inference. (e) Cladogenesis rate using the time scaled trees arising from the maximum parsimony analysis and extinction rate. The light grey outline represents the range of values, encompassing all most-parsimonious trees. (f) Number of marine reptile-bearing and ichthyosaur-bearing formations throughout the Cretaceous. (g) Proportion of marine reptile-bearing formations containing ichthyosaurs throughout the Cretaceous, with calculation of a 95% confidence interval. (f,g) Indicate ichthyosaurs disappeared in a two-phase extinction during the Cenomanian, and that this extinction is not biased by the fossil record: ichthyosaurs rarefy and disappear during a time of excellent recovery potential. Full size image

Figure 4: A two-phase extinction for ichthyosaurs. (a) Biostratigraphic ranges of the last ichthyosaur taxa. Questions marks indicate uncertainty of the stratigraphic range of the material from Stoilensky quarry (western Russia). Thin lines indicate uncertain but probable occurrence of taxa, based on the presence of compatible remains. See Supplementary Note 1 for the details and discussion on the specimens considered in the bracketed numbers. (b) Evolution of worldwide ichthyosaur diversity (at the species level in black and at the lineage level in orange) for each bin considered (Late Albian, earliest Cenomanian, Early Cenomanian, Mid-Cenomanian, Late Cenomanian, Turonian. The lighter colour indicates how the curve would look in Platypterygius campylodon is not regarded as a valid entity. (c) Evolution of the number of feedings guilds colonized, based on the results from the cluster analysis of ecological data. Note the sharp reduction after the earliest Cenomanian. (d) Extinction rate at the boundaries of each bin. Per-lineage extinction rates≥40% are recorded in the two phases of ichthyosaur extinction. Full size image

Ecological diversity of ophthalmosaurids

Cluster analysis of ecological data (Supplementary Table 12, Supplementary Methods and Supplementary Data 7) recovers three main ecomorphological groups, further divided into a range of subgroups, and supported by significant approximated unbiased P values (Fig. 2). The first group is characterized by minute recurved teeth with a smooth and slender crown and no detectable wear. Two of them are ophthalmosaurines, with a large sclerotic aperture, and preserved gut content in one of them (Ophthalmosaurus natans) consists of only soft, unshelled coleoid remains28. We propose that these ichthyosaurs had a restricted diet of small, soft-prey items and were unlikely to process large prey items into smaller pieces; we term this group soft-prey specialists (which probably also incorporate the ‘specialized ram feeders’ of ref. 11). The second group is the most speciose, contains only platypterygiine ichthyosaurs, and is characterized by large and robust teeth, heavy apical wear and quite often a robust (dorsoventrally deep, which better resists torsional stresses29) rostrum and possibly a relatively shorter symphysis. One member, ‘Platypterygius australis’13, has been found with remains of birds, turtles and fishes in its gut. We propose this group fed on a wide range of prey, including other vertebrates; we term this group apex predators. All species currently referred to as Platypterygius except ‘Platypterygius sachicarum’ unite in this cluster. This grouping could indicate that these species superficially resemble each other because of ecology rather than shared ancestry. The third group contains medium-sized ichthyosaurs with a slender rostrum, bearing small teeth with a robust crown and slight wear; we propose this group preyed on a wide range of small animals. Because they share features with the two other groups, we term this group generalists. Subgroups of the cluster are supported by significant P values as well, but do not appear to be supported by radically distinct features. If anything, these groupings probably reflect subtle differences that could allow niche partitioning between coeval taxa. The stratigraphic distributions and counts of feeding guilds through time should be a reliable measure of ecological disparity regardless of the accuracy of our interpretations of their specific diets.

The stratigraphic distributions of our feeding guilds suffer from the same biases as observed diversity and both are broadly correlated. For example, the absence of multiple co-occurring guilds in the Berriasian–Hauterivian and Aptian–Lower Albian intervals likely reflects the poor fossil records of these intervals. Mitigating bias is difficult here, as reconstruction of ancestral ecological niches defies the principle of ecological convergence, which was widespread in marine tetrapods10,30. It is, however, possible to infer the presence of a guild by using the features that appear relevant to identify the different clusters. This approach leads us to propose that the Albian–Cenomanian boundary fauna we investigated in Stoilensky quarry, western Russia (Supplementary Figs 16–19; Supplementary Table 13 and Supplementary Methods) contains taxa occupying three distinct ecological niches. The ecological diversity of Cretaceous ichthyosaurs was high, as is especially apparently at times of better sampling. This ecological diversity declined abruptly during the early Cenomanian, despite the continued sampling of ichthyosaur specimens from all major geographic regions sampled in the late Albian and the increased preservation potential (Figs 3 and 4 and Supplementary Table 14).

Effect of sampling and environmental changes

We used generalized least squares regression with a first-order autoregressive model and pairwise correlations to test the relationship between various biodiversity dynamics metrics, and environmental and sampling proxies (Supplementary Tables 15 and 16). All tests found poor correlations between sampling metrics and diversity variables (Supplementary Tables 17–19 and Supplementary Data 8 and 9). Akaike weights systematically place most sampling metrics among the variables with the lowest explanatory power for most diversity variables. This result suggests that the use of phylogeny-informed diversity metrics yield a signal that at least partially redresses sampling biases (but see ref. 31, as phylogenetic diversity estimates can fill ranges backwards but not forwards and are therefore prone to edge effects). The general absence of correlation between rates (cladogenesis, evolutionary and turnover), except extinction and sampling metrics is also interesting, especially in the light of recent analyses finding strong correlations between standing diversity and sampling metrics (for example, see ref. 32); this suggests that future analyses should focus on the dynamics of diversity rather than on raw values.

Broadly, bin-averaged environmental data, which represent interval-specific mean environmental conditions, do not appear to explain the diversity metrics for Cretaceous ichthyosaurs and no robust signal common to all four analyses could be recovered (Supplementary Tables 17–19). On the contrary, climate volatility variables (∂180 and ∂13C variances) are the best or among the best models for predicting the extinction rates and the per-lineage extinction rates in both data sets. A strong correlation is also found in the pairwise tests between the per-lineage extinction rates and the variances of both the ∂18O and the short-term eustasy in the full data set. It is crucial to stress the importance of the extinction of ichthyosaurs in polarizing these correlations. Indeed, analyses of the full data set yielded a much larger number of significant/non-negligible correlations, especially with climate instability variables.

Confidence in the timing and tempo of extinction

Counts of marine reptile fossil bearing formations across the Middle Cretaceous (Albian–Turonian) are among the highest of the Cretaceous, so the Cenomanian last occurrences of ichthyosaurs and their main Cretaceous ecomorphs occur during a well-sampled interval (Fig. 3). During this span, the proportion of marine reptile-bearing formations yielding ichthyosaurs decreased from 84% in the Albian to 19% in the Cenomanian and to 0% in the Turonian. Given the presence of n=26 marine reptile-bearing formations in the Turonian, the probability of observing zero Turonian ichthyosaur fossils given an occurrence frequency of 0.19 per formation is (1–0.19)N, or 0.004. Furthermore, given the observation of zero ichthyosaurs in 26 Turonian marine reptile-bearing formations, the occurrence frequency of Turonian ichthyosaurs would have to be 0.109 (that is, <10.9%) or less to give a probability of at least 0.05 of finding zero Turonian ichthyosaur fossils. To obtain a high probability (0.5) of observing no ichthyosaurs in this many sampling opportunities, the occurrence frequency would need to be no more than 0.026 (that is, <2.6%). Thus, if not actually extinct, to remain undiscovered, Turonian ichthyosaurs would need to be rare to the degree that they were ecologically insignificant. On the basis of these observations, it is likely that our estimate of the timing of ichthyosaur extinction is adequate at the timescale of our study.