Intraspecific variation in fossil vertebrate populations: Fossil killifishes (Actinopterygii: Cyprinodontiformes) from the Oligocene of Central Europe
Article number: 19.2.14A
Copyright Society for Vertebrate Paleontology, May 2016
Submission: 14 January 2016. Acceptance: 13 April 2016
A quantification of intraspecific variation in morphological traits is necessary not only as a basis for taxonomic work but also to understand a basic aspect of evolution. Comparisons among species could reveal differences in plasticity in development among them and even give clues on evolvability. Studies of this kind are rare for extinct species of vertebrates given the lack of adequate samples, but there are notable exceptions. Morphometric and meristic data were collected for three species of fossil killifish in order to quantify intraspecific variation: 67 specimens of Prolebias rhenanus from the Lower Oligocene of Baden-Württemberg, 40 specimens of Pr. stenoura from the Lower Oligocene of Puy-de-Dôme, and 141 specimens of Paralebias cephalotes from the Upper Oligocene of Aix-en-Provence. Nearly identical patterns of intraspecific variation exist between the two species of Prolebias. Fin base lengths and precaudal lengths of the vertebral column are the most variable traits in both species, followed by pterygiophore counts, then other axial length measurements and, least variable, vertebral counts. In neither species was there a significant difference in observed variation between fin and vertebral or meristic and morphometric traits. The only significant correlation shared between the two species is the positive relationship between caudal length of the vertebral column and length of the anal fin base. Precaudal length of the vertebral column is less variable in Paralebias than in Prolebias, while precaudal vertebral count is more variable, in absolute values of the coefficient of variation. Variability in elongation of precaudal vertebrae may be the underlying cause of the absence of correlation between decreased variation in precaudal length of the vertebral column and increased variation in precaudal count in Paralebias cephalotes. We report more similar patterns of variation among Prolebias congeners than between Prolebias and Paralebias, suggesting that trait variability is changing over evolutionary time in this actinopterygian lineage.
Linda Frey. Palaeontological Institute and Museum, University of Zurich, Karl-Schmid-Str. 4, CH-8006, Switzerland.
Erin E. Maxwell. Staatliches Museum für Naturkunde, Rosenstein 1, DE-70191 Stuttgart, Germany.
Marcelo R. Sánchez-Villagra. Palaeontological Institute and Museum, University of Zurich, Karl-Schmid-Str. 4, CH-8006, Switzerland. (corresponding author)
Keywords: Atherinomorpha; morphology; variability; taxonomy; skeleton; modularity
Final citation: Frey, Linda, Maxwell, Erin E., and Sánchez-Villagra, Marcelo R. 2016. Intraspecific variation in fossil vertebrate populations: Fossil killifishes (Actinopterygii: Cyprinodontiformes) from the Oligocene of Central Europe. Palaeontologia Electronica 19.2.14A: 1-27. https://doi.org/10.26879/628
Copyright: © 2016 Society of Vertebrate Paleontology. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Macroevolutionary patterns of disparity and diversity are tied to the evolution of variation (Simpson, 1953; Mayr, 1963; Hallgrímsson and Hall, 2005; Webster, 2007, 2014; Hunt, 2007), which can be studied in geological time (Webster, 2007; De Baets et al., 2013). Examination of phenotypic variation within populations is essential for taxonomy because non-consideration of such can lead to taxon over-splitting (Hughes and Labandeira, 1995; Labandeira and Hughes, 1994). To study intraspecific variation in palaeontology, well-preserved and large samples with adequate stratigraphic information are desirable, in order to minimize sampling biases and the effect of time-averaging (Schaeffer et al., 1972; Bookstein et al., 1978; Petry, 1982; Behrensmeyer, 1982). However, comparisons between variation in extinct and extant populations of invertebrates and vertebrates show that palaeontological samples were not strongly affected by time-averaging (Bell and Legendre, 1987; MacFadden, 1989; Bush et al., 2002; Hunt, 2004a, b). Studies of variation in extinct populations or species are more common when studying invertebrates, such as trilobites (Hughes and Labandeira, 1995; Labandeira and Hughes, 1994; Webster, 2007, 2014; Hopkins, 2011), ammonoids (Hohenegger and Tatzreiter, 1992; Korn and Klug, 2007; Monnet et al., 2010; De Baets et al., 2013), and crinoids (Lane, 1963; Meyer and Ausich, 1997). Among fossil tetrapods, studies on intraspecific variation have been conducted for example for dinosaurs (Raath, 1990; Bever et al., 2011; Foth and Rauhut, 2013), ichthyosaurs (Maxwell, 2012), rodents (Renaud et al., 2006; Lazzari et al., 2010) and horses (MacFadden, 1997). Several studies on variation in extinct populations of fishes have been carried out during the last three decades, mostly concerning microstratigraphic changes in variation of meristic and morphometric characters of different body parts, or phenotypic variation as it relates to taxonomically informative characters (Bell and Haglund, 1982; Bell et al., 1985; Bell and Legendre, 1987; Cloutier, 1997; Smith, 1987; McCune, 1990, 1996; Barton and Wilson, 1999; Micklich and Klappert, 2004; Grande, 2010; Table 1).
We chose fossil populations of cyprinodontiforms as a study system in which to examine phenotypic variation in palaeontology. Cyprinodon-tiformes represents a speciose clade of teleosts, including extant and extinct taxa (approximately 1200 species, 125 genera) that occur in freshwater and brackish waters of Europe, Africa, and Asia (Nelson, 2006; Costa, 2012). The skeletons of many species of Oligocene and Miocene killifishes of Europe are well-preserved and articulated, present in many localities in very high numbers (Gaudant, 2013). As such, they are a good subject for studies of phenotypic variation. Fossil populations of valenciids such as Prolebias rhenanus Gaudant, 1981a and Pr. stenoura Sauvage, 1874 and of poeciliids such as Paralebias cephalotes (Agassiz, 1839) in particular are represented by large numbers of individuals from restricted stratigraphic and geographic intervals in France and Germany (e.g., Pa. cephalotes: Figure 1).
Studies of variation in extant killifishes can provide the bases for evaluation of fossils. Recent populations of closely-related species are preferred study objects for the examination of morphological differentiation within and among populations because of their occurrence in different environments and their separation by natural barriers (e.g., Hubbs and Miller, 1965; Chernoff and Hall, 1979; Parenti and Tigano, 1993; Tigano and Ferrito, 1984, 1985; Tigano et al., 1999, 2001; Doadrio et al., 2002; Ferrito et al., 2003, 2007; Garcìa et al., 2009; Costa, 2010, 2011; Reichenbacher and Reichard, 2014; Reichenbacher et al., 2007). However, the examination of variation in extant populations can provide only a snapshot of morphological variation at the tips of the phylogeny. In order to assess the manner and rate at which variation has changed through time within a single lineage, palaeontological data are essential.
The aim of this study is to quantify intraspecific variation in meristic and morphometric characters, and to examine similarities in the distribution of this variation across multiple species in a clade. We compare the degree of variation in different regions of the axial skeleton (fins versus vertebral column). We hypothesize that fin characters are more variable than vertebral characters across all species, as high levels of variability in late-forming and peripherally located serially repeated elements have been reported in both developmental and palaeontological studies (Cloutier et al., 2010; Barton and Wilson, 1999). In addition, we examine the relationship between meristic and morphometric variation. Although logically meristic variation should result in an equal degree of morphometric variation, the relationship between these is rarely explicitly assessed. The traits we examine are relatively easy to obtain and are commonly reported in the literature. These include vertebral count (Winkler et al., 2012; Maxwell and Wilson, 2013; Aguirre et al., 2014) and median fin length (Webb, 1984), which pertain directly to fish body shape and thus ecomorphology.
MATERIALS AND METHODS
In order to obtain an estimate of variability in phenotypic features, morphometric and meristic data (characters adopted from Barton and Wilson  and Hubbs and Lagler ) were collected for three species of fossil killifish: Prolebias rhenanus Gaudant, 1981, Pr. stenoura Sauvage, 1874, and Paralebias cephalotes (Agassiz, 1839) (Figure 2; Appendix). Each of these species of killifishes occurs at high abundance in geographically restricted areas. We sampled the following meristic characters: total vertebrae (TV), precaudal vertebrae (PV), caudal vertebrae (CV), dorsal pterygiophores (DP), and anal pterygiophores (AP). To minimise error in meristic variables, we counted meristic variables twice for each specimen, once from the anterior and once from the posterior end of the column (following Barton and Wilson, 1999). We did not include counts of fin rays as they were often badly preserved and displaced. We also collected measurement data (in mm), including standard length (SL; from the anterior part of the head to the end of the hypural plate), total length of vertebral column (TVL; from the first precaudal vertebra to the posterior end of the hypural plate), length of precaudal and caudal regions of the vertebral column (PCL and CL; from the first to the most posterior precaudal vertebrae and from the most anterior caudal vertebra to the posterior end of the hypural plate, respectively), and length of dorsal and anal fin bases (DPL and APL) (Table 2, Figure 3, Figure 4). To avoid damage to the fossils and to obtain more accurate measurements for small specimens, we took photos of all specimens and from them obtained measurements using the software Photoshop CS6 (Adobe Systems Incorporated, San Jose, CA, USA). We used the line tool to precisely align curves and lines to the different length parameters and later, we could easily measure the length of these shapes at the scale in the photographs. Due to incompleteness or disarticulation, not all data could be collected for every specimen.
Sixty-seven specimens of Prolebias rhenanus from the Lower Oligocene of the locality “Rüssgraben bei Kleinkems” (Baden-Württemberg, Germany) were included in the study (Figure 2.1). These were originally from the collection of Mathieu Mieg and are housed in the Naturhistorisches Museum of Basel, Switzerland. Mieg (1892) reported the occurrence of those fossil fishes within two thin layers consisting of “Plattiger Steinmergel” at a section at Rüssgraben bei Kleinkems. These layers are thin, not exceeding 0.15 m in thickness, and are separated by approximately 1 m of sediment (Mieg, 1892). Prolebias rhenanus has been hypothesized to tolerate fresh to brackish water conditions (Gaudant, 1981a) and inhabited a shallow saline lake periodically filled by freshwater from precipitation (Lutz, 1997).
We also sampled 40 specimens of Prolebias stenoura from the Lower Oligocene of Puy-de-Dôme, France, housed in the Natural History Museum of London (NHM) since the nineteenth century (Gaudant, 2012; Figure 2.2). The precise stratigraphic position of these specimens is unknown, but the specimens of the Croizet Collection, to which many of the specimens are attributed, were found in different lacustrine sediments around Corent (Giraud, 1902; Pécoil, 1938; Gorin, 1975). Prolebias stenoura occurred in a shallow meromictic lake with fresh to slightly brackish water conditions at the surface (Gaudant, 2012).
Lastly, we sampled 141 specimens of Paralebias cephalotes from the Upper Oligocene of Aix-en-Provence (Bouche-du-Rhône, France), housed in the Natural History Museum of London (Figure 2.3). Paralebias cephalotes was recovered from 12 different horizons during a modern excavation at Aix-en-Provence (Gaudant, 1978). The abundance of the species and the associated fauna fluctuated throughout the 1.6 m section. Variable species abundance and faunal composition are hypothesized to reflect changes in salinity in the lake, and Pa. cephalotes appears to have inhabited freshwater to slightly brackish environments (Gaudant, 1978).
Morphological measurements were log-transformed to equalize variance between different measurements, and all measurement data were corrected for size using multiple regression with the skull length as the independent variable. Size correction is necessary to exclude predictable ontogenetic changes in morphometric traits (McCoy et al., 2006). We selected multiple regression on skull length to standardize the data versus simply standardizing measurements as fractions of total or standard length because body length is not independent of length of the vertebral column, the trait of interest. As meristic traits are fixed during early ontogeny, they are independent of body size and so size-correction was not performed. To obtain an estimate of trait variability, we calculated the coefficients of variation (COV: standard deviation divided by the trait mean) for each character using log-transformed and size-corrected data. We tested for overall differences in variation between fin characters and vertebral characters, and between morphometric characters and meristic characters using a Mann-Whitney U-test. Pairwise correlations between morphometric and meristic and fin and vertebral characters were examined using Spearman’s rho. All analyses were performed using the statistical program PAST (Hammer et al., 2001).
Observed variation of characters
We obtained similar vertebral counts to those presented in Gaudant (2012) in Prolebias stenoura, but the range of dorsal and anal fin pterygiophore counts was much greater in our work (Table 2). In all the counts of Problebias rhenanus and Paralebias cephalotes, we found broader ranges than in previous studies (Gaudant, 1981a, b, 2009). The differences in ranges are possibly attributable to different sample size.
In Prolebias rhenanus, lengths of the precaudal vertebral column and of the fin bases show the most variation (COV PCL = 10.8, COV DPL = 10.8, COV APL = 9.8; Table 3). This is followed by variation in pterygiophore counts and axial length variables (COV DP = 8.8, COV AP = 7.5, COV CL = 6.4, COV SL = 5.5, COV TVL = 5.2). Vertebral counts were the least variable characters in the sample; the number of caudal vertebrae was more variable than the number of precaudal vertebrae (COV TV = 2.4, COV PCV = 2.9, COV CV = 3.5). Coefficients of variation between fin and vertebral characters are not significantly different (mean ranks 3.1 and 2.5, P = 0.07), nor were coefficients of variation between count and length variables (mean ranks 1.9 and 4.1, P = 0.12).
Based on the data presented here, length of the dorsal and anal fin bases was most variable (COV APL = 18.4, COV DPL = 16.8; COV PCL = 13.5, see Table 3) followed by pterygiophore counts and axial length measurements (COV DP = 10.3, COV AP = 8.8, COV SL = 6.9, COV TVL = 8.5, COV CL = 9.0) in Prolebias stenoura. Vertebral count variables showed the low coefficients of variation and with caudal counts being the most variable (COV TV = 2.2, COV PCV = 2.9, COV CV = 3.6). Morphometric characters were not significantly more variable than meristic characters (mean ranks 4.3 and 1.7, P = 0.06), and differences in variation between fin and vertebral characters were not significant (mean ranks 3.0 and 2.5, P = 0.11).
In Paralebias cephalotes, lengths of the fin bases are the most variable traits, followed by pterygiophore counts (COV DPL = 24.0, COV APL = 13.8, COV DP = 13.5 and COV AP = 10.3). Measurements and counts of the precaudal vertebral column are the most variable vertebral measures (COV PCL = 7.7 and COV PCV = 5.9), followed by total and caudal vertebral characters (COV SL = 3.5, COV TVL = 3.9, COV CL = 4.6, COV TV = 3.4 and COV CV = 4.7). Coefficients of variation of fin characters are higher than those of vertebral characters (mean ranks 3.4 and 2.1, P = 0.009). Mean ranks of morphometric and meristic characters do not differ significantly from each other (mean ranks 3.7 and 2.6, P = 0.90).
Correlation of characters
In Prolebiasrhenanus the number of precaudal vertebrae is negatively correlated with anal pterygiophore count (correlation coefficient: S = -0.54, P = 0.02). Precaudal length and caudal length of the vertebral column are both positively correlated with length of the fin bases (PCL: S = 0.36, P = 0.004; S = 0.3, P = 0.01; CL: S = 0.27, P = 0.03; S = 0.58, P = 9.18×10). The relationship between length of the dorsal fin base and number of dorsal pterygiophores is significant and positive (S = 0.58, P = 0.0003) (Table 4).
In Prolebias stenoura, caudal length of the vertebral column is positively correlated with length of the anal fin base (S = 0.32; P = 0.04). The relationship between the base of the anal fin and the number of anal pterygiophores is significant and positive (S = 0.43, P = 0.01) (Table 5).
In Paralebias cephalotes, fin base lengths are positively correlated with all vertebral length traits. Caudal length is negatively correlated with the number of precaudal vertebrae (S = -0.49, P = 0.04), but positively correlated with number of caudal vertebrae (S = 0.25, P = 0.002). The length of the dorsal fin base is significantly correlated with the number of dorsal pterygiophores (S = 0.46, p-values = 9.44×10), and the length of the anal fin base is significantly correlated with the number of anal pterygiophores (S = 0.31, P = 7.02×10) (Table 6).
Nearly identical patterns of intraspecific variation exist between the two species of Prolebias. Length of the fin base and of precaudal parts of the vertebral column are the most variable traits in both species, followed by pterygiophore counts, then other axial length measurements and, least variable, vertebral counts. The magnitude of the observed variation for most traits, including measurements and pterygiophores counts, is greater in Pr. stenoura , but the coefficient of variation for the vertebral counts are identical in both species. In neither species was there a significant difference in observed variation between fin and vertebral or meristic and morphometric traits. In the samples of both species, there is a positive relationship between caudal length of the vertebral column and length of the anal fin base. Interestingly, although Pr. stenoura shows relatively greater amounts of variation for most traits, this variation appears to be stochastically distributed: for the trait combinations tested, Pr. rhenanus exhibits more and stronger covarying trait relationships.
The pattern of variation observed in Paralebias cephalotes is similar to Prolebias, with one major exception: precaudal length (COV PCL = 7.7) is less variable in Paralebias while precaudal vertebral count (COV PCL = 5.9) is more variable. However, as it was the case in Prolebias, this variation appears to be randomly distributed: precaudal length and the number of precaudal vertebrae are not significantly correlated, suggesting that the decrease in variation observed in the first and the increase in variation observed in the second are not due to trait integration. In addition, a significant difference in variability was detected between fin and vertebral characters, with vertebral characters being less variable in Pa. cephalotes. The relative amount of variation observed was slightly, but not dramatically greater in Pa. cephalotes (mean ranks 3.7 and 2.6, P = 0.90) than in Pr. stenoura (mean ranks 3.0 and 2.5, P = 0.11), and may be attributed to larger sample sizes in the former.
Decreased variation in precaudal length of the vertebral column and increased variation in precaudal count in Paralebias cephalotes in the absence of any correlation between the two traits suggests an underlying cause: variability in elongation of precaudal vertebrae. This pattern clearly does not extend into the caudal region, where a significant relationship exists between caudal length and number of caudal vertebrae, as reported in an extensive and phylogenetically broad examination of bony fishes species (Lindsey, 1975). Elongate fishes extend the vertebral column either through elongation of the vertebral centra or through addition of vertebrae (Ward and Mehta, 2010), and our results imply that variation in both vertebral number and vertebral length may be present in populations.
In Prolebias spp. caudal vertebral counts (COV CV = 3.5 for Pr. rhenanus and 3.6 for Pr. stenoura, respectively) are significantly more variable than precaudal counts (COV PCV = 2.9 for both species). The pre-ural caudal region of the vertebral column in fishes is hypothesized to be more variable than the precaudal region, as segmentation proceeds from anterior to posterior (Itazawa, 1963; Nagiec, 1977; Lindsey, 1988; Grande and Bemis, 1998; Barton and Wilson, 1999; Aguirre et al., 2014), and most actinopterygians add vertebrae to the caudal region preferentially (Ward and Mehta, 2014), suggesting increased variability in this region. However, this is not a universal rule: some actinopterygians do add vertebrae preferentially to the abdominal region (Mehta et al., 2010; Maxwell and Wilson, 2013), and this may result in increased variability in abdominal counts within species. Sexual dimorphism may also increase observed variation in abdominal vertebral counts preferentially relative to caudal counts due to selection for increased abdominal volume in females (Lindsey, 1975).
Intraspecific variation in vertebral counts is correlated with a multitude of factors in teleosts, including life history (McDowall, 2003), sex (Aguirre et al., 2014; Lindsey, 1975), habitat (Shikano and Merilä, 2011), and temperature/latitude/altitude (Barriga et al., 2013; Baumann et al., 2012; Hice et al., 2012; McDowall, 2003; Yamahira et al., 2006; Yamahira and Nishida, 2009). Heritability of vertebral numbers is high, but phenotypic plasticity is well documented (Lindsey, 1988; Yamahira and Nishida, 2009). Differences in sample size, multi-year sampling effects, salinity, and other habitat characteristics may influence the absolute amount of variation observed, as has been reported in other teleosts (e.g., McDowall, 2003; Shikano and Merilä, 2011), including killifishes (Maltagliati et al., 2003). Prolebias rhenanus and Paralebias cephalotes inhabited brackish waters with fluctuating salinity content, whereas Pr. stenoura inhabited freshwater lakes. As the pattern of variation between Problebias spp., which lived in different water conditions, is similar, differences in salinity do not seem to have affected such variation. Moreover, the number of precaudal vertebrae in fossil killifishes was difficult to observe, since the most anterior vertebrae are often badly preserved or covered by the skull (Gaudant, 1981a), and thus measurement error cannot be eliminated as a source of increased variation.
Variability between fin and vertebral characters is similar in Prolebias spp. (Prolebias rhenanus : mean ranks 3.0 and 2.5, P = 0.11; Pr. stenoura : mean ranks 3.0 and 2.5, P = 0.11), but Paralebiascephalotes (mean ranks 3.7 and 2.6, P = 0.90) shows greater variability in characters pertaining to the median fins. However, even in Prolebias spp. traits pertaining to the dorsal and anal fins are extremely variable ( Prolebias rhenanus : COV APL, AP, DPL, DP = 9.8, 7.5, 10.8, 8.8; Pr. stenoura: COV APL, AP, DPL, DP = 18.4, 8.4, 16.8, 10.3). Although descriptive statistics pertaining to morphological variation (i.e., mean, standard deviation) are rarely presented for extant cyprinodontiforms, those few data that are available are consistent with our observations. For instance, the COV TV and the COV of axial length measurements are less than those of both dorsal and anal fin ray counts in males of the extant poeciliid Gambusia quadruncus (Langerhans et al., 2012); females appear to be more variable than males but all COV values fall into the range reported in our fossil samples (e.g., COV (TV) = 2.4%). In three goodeid species belonging to Xenoophorus, length measurements pertaining to vertebral regions also had on average lower coefficients of variation than the lengths of the fin bases, with the length of the anal fin base showing the highest COV and the length of the axial skeleton anterior to the dorsal fin showing the least variation in all species. Count data were not available. As in Gambusia, females showed overall slightly higher amounts of variation than males (Fitzsimons, 1979).
Variation in vertebral counts should theoretically be lower than in pterygiophore (proximal radial) counts in fishes, based on a more terminal position of the latter in the developmental sequence (both in terms of patterning and ossification) resulting in an increased number of ways in which variation may be introduced (Lindsey, 1988). This effect may be amplified in fossil fishes, since pterygiophores ossify relatively late in ontogeny (e.g., Bird and Mabee, 2003; Grünbaum et al., 2012) and thus may not be preserved in smaller specimens even when present. Higher variability in pterygiophore counts than vertebral counts is supported in a species of catastomid (Barton and Wilson, 1999). Studies on variation in fishes have reported that fin traits are more variable than vertebral ones in general (Cloutier et al., 2010; Barton and Wilson, 1999; MacGregor and MacCrimmon, 1977). Median fins rely on the same positioning cues as the vertebral column early in development (Freitas et al., 2006) and later in development articulate with the neural and haemal spines (Figure 2) (Bird and Mabee, 2003). This suggests that, to a certain degree, the two sets of traits should be correlated: as the vertebrae grow longer, the bases of the fins are also constrained to become longer, and indeed this is what is observed in our studied samples, with all species showing a positive correlation between the lengths of at least one of the fin bases and the vertebral column. However, the lengths of the fin bases are also related to the number of pterygiophores, and this appears to be the underlying cause of observed variation in fin characters. Pterygiophores ossify late in development (Fischer-Rousseau et al., 2009; Cloutier et al., 2010; Grünbaum et al., 2012), and environmentally induced plasticity is observed in their timing of ossification (Cloutier et al., 2010; Grünbaum et al., 2012) so it is uncertain whether variable ossification rather than meristic variability is promoting variation in fin characters.
In conclusion, our data suggest similarities in patterns of variation among closely related species, with possible divergence of trait variability between ‘families’ (Poeciliidae - Paralebias vs. Valenciidae - Prolebias : Costa, 2012; Gaudant, 2013). More thorough sampling within Cyprinodontiformes is needed to evaluate the time-scales over which such shifts occur. Divergence in patterns of trait covariance have previously been reported over a range of time and spatial scales (population: Game and Caley, 2006; stratigraphic: Maxwell and Dececchi, 2013; phylogenetic: Goswami et al., 2014), and variability in the amount of morphological variation present has been shown in a general way between populations (Game and Caley, 2006). Our results suggest that not only can the variance-covariance matrix be restructured, and different amounts of absolute variation be present (Wilson, 2013), but the variability of specific traits also changes over evolutionary time. The ~10% absolute variation in vertebral numbers among individuals we found may have influenced locomotory performance in the populations studied (Brainerd and Patek, 1998; Spouge and Larkin, 1979), although the relationship between vertebral numbers and locomotory performance is complex.
We thank the curators L. Costeur (Naturhistorisches Museum, Basel) and E. Bernard (Natural History Museum, London) for access to important collections; C. Meyer from the Naturhistorisches Museum Basel, for important input at the beginning of the project on the geology of the localities with the studied fossils, and for information on collections at the Museum in Basel, and two anonymous reviewers who made useful suggestions we implemented. This project was supported by funding from the Swiss National Science Foundation (SNF) Sinergia program, granted to MRS-V, and a collaboration with Walter Salzburger and Heinz Furrer (CRSII3-136293).
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