Phenotypic Changes Across a Geographic Gradient: The Case of Three Sympatric Dolphin Species

Abstract

Phenotypic changes in the mammalian mandible can occur at different spatial and temporal scales. We investigated mandibular size and shape variation in three extant closely related dolphins (Cetacea, Odontoceti): Tursiops truncatus, Stenella coeruleoalba and Delphinus delphis in order to test the hypothesis that similar phenotypic changes occur across the same geographical gradient. Our data included 219 specimens representative of the following geographic locations: the Mediterranean Sea, the eastern north Atlantic and the North Sea. Each mandibula was photographed laterally and spatial positioning of eight homologous 2D landmarks was recorded. After applying generalised Procrustes analysis (GPA), intraspecific variation was first investigated between sexes and among populations to allow further pooling of samples. Size and shape differences among populations and species were investigated through multivariate ordination techniques (PCA), Procrustes ANOVA and allometric analyses. In all three species, Mediterranean populations clearly differed in mandible shape from the extra-Mediterranean ones. Among the three, the direction of geographic phenotypic changes was significantly similar in the striped and common dolphin, while the bottlenose dolphin was the most divergent species, differing both in size and allometric trajectory. Shape variation of the two former species highlighted a morphological convergence in the Atlantic, and a phenotypic divergence in the Mediterranean. Shape differences among the three dolphin species were interpreted in the light of different prey preferences, feeding strategies and habitat partitioning to avoid direct competition.

Introduction

The mammalian mandible represents a model for the evolution of complex structures (Atchley and Hall 1991) and its morphology has been widely studied to reconstruct feeding behaviour of extant and fossil species (Meloro 2011; Figueirido et al. 2009; van Heteren et al. 2016; Raia 2004; Raia et al. 2010; Meloro et al. 2008; Piras et al. 2010, 2013), to investigate relationships with ecological adaptation and phylogenetic history (Barroso et al. 2012), to assess geographic variation (Meloro et al. 2017) and getting insights into its modular structure (Klingenberg et al. 2003; Monteiro and Nogueira 2010; Guidarelli et al. 2014). In spite of its structural simplicity, studies on both terrestrial (Klingenberg et al. 2003; Raia 2004; Meloro et al. 2008, 2011, 2015a, 2015b, 2017; van Heteren 2009; van Heteren et al. 2016) and aquatic mammals (Barroso et al. 2012; Guidarelli et al. 2014; Heyning and Perrin 1994; Nummela et al. 2004; Wang et al. 2000) proved that mandibular morphology provides critical insights into species taxonomy, ecology and evolutionary history. However, in cetaceans, mandibular variation between and within species has been little explored. Barroso et al. (2012) analysed mandibular shape across all major odontocetes lineages, while Guidarelli et al. (2014) focused on interspecific variation and modularity in three Mediterranean dolphins: the short-beaked common dolphin (Delphinus delphis), the striped dolphin (Stenella coeruleoalba) and the bottlenose dolphin (Tursiops truncatus). These small cetaceans belong to the subfamily Delphininae, family Delphinidae, that currently comprises 37 species (Committee for Taxonomy 2016). The Delphininae likely arose from an extremely rapid radiation during mid to late Miocene, leading to unresolved evolutionary relationships among the most recently diverged species of the subfamily Delphininae (Slater et al. 2010; Kingston et al. 2009; McGowen et al. 2009; McGowen 2011; Steeman et al. 2009; Amaral et al. 2012; Perrin et al. 2013).

The common, striped and bottlenose dolphin are widely distributed in tropical and temperate waters of the Pacific, Atlantic and Indian Oceans, and in most seas of the world including the Mediterranean Sea. The Mediterranean is the deepest and the largest basin on Earth and it is a marine biodiversity hotspot with high percentages of endemic species (Bianchi and Morri 2000; Danovaro and Pusceddu 2007). This semi-enclosed basin is generally characterized by high sea temperature, high salinity, great seabed topographic variability and homothermy, with water temperatures remaining constant starting from 300 to 500 m to the bottom (Coll et al. 2010). The presence of diverse oceanographic dynamics and water circulation patterns result in high variability in productivity in both space and time (Otero and Conigliaro 2012). The Atlantic Ocean has denser and cooler waters, characterized by low salinity and lower sea temperatures, decreasing with depth. The Strait of Gibraltar is the narrow and shallow passage between the Mediterranean and the Atlantic Ocean. Excluding the Suez Canal, it constitutes the only source of oceanic water and, throughout the history, it has been the main source of biota to the Mediterranean Sea (Coll et al. 2010). Many studies tested the hypothesis of the Strait of Gibraltar acting as a phylogeographical barrier for both invertebrates and vertebrates and three main phylogeographic scenarios were presented: lack of population structure, Atlantic and Mediterranean separation and genetic boundaries not associated with Gibraltar (Quesada et al. 1995; Pérez-Losada et al. 2002; Duran et al. 2004; Cimmaruta et al. 2005; Patarnello et al. 2007). When the Atlantic-Mediterranean transition is analysed at a finer geographical scale, some species show a drastic genetic change that corresponds with an oceanographic front located between Almeria (Spain) and Oran (Morocco), called the Almeria-Oran Front. Specifically, this phenomenon was observed in both invertebrate and vertebrate species, including Sepia officinalis (Pérez-Losada et al. 2002), Mytilus galloprovincialis (Quesada et al. 1995), Paracentrotus lividus (Duran et al. 2004), Dicentrarchus labrax (Naciri et al. 1999) and Merluccius merluccius (Cimmaruta et al. 2005; Patarnello et al. 2007).

As for small delphinids, genetic studies have identified population boundaries between Mediterranean and North Atlantic populations (Natoli et al. 2008, 2005; Garcia-Martinez et al. 1999, 1995; Gaspari et al. 2007; Bourret et al. 2007). In Delphinus delphis, mtDNA revealed significant genetic differences between the Alboran Mediterranean population and the Atlantic Ocean (Galicia and Portugal) (Natoli et al. 2008). Both mtDNA (Garcia-Martinez et al. 1995, 1999) and nuclear markers (Valsecchi et al. 2004; Gaspari et al. 2007; Bourret et al. 2007) revealed a distinct separation between Mediterranean and North Atlantic stocks of the striped dolphin Stenella coeruleoalba. Natoli et al. (2005) found a clear genetic differentiation between populations from the Black Sea to Scotland (North-East Atlantic Ocean) for the bottlenose dolphin T. truncatus. Most important differences were found between Scotland and the southern North Atlantic, and between the Mediterranean and the Black Sea. Genetic differences were also observed in mtDNA between the western Mediterranean Tursiops populations and the adjacent Atlantic ones (Galicia and Portugal), supporting evidences of a genetic boundary at the Almeria-Orán front. Differences in oceanographic parameters (ocean floor topography, surface salinity, temperature and productivity) were suggested as potential drivers of genetic structure (Natoli et al. 2005).

A high degree of morphometric differentiation was found among small delphinid species across different geographical areas (Bell et al. 2002; Wang et al. 2000; Perrin 1984, 1975; Heyning and Perrin 1994). Regarding the Mediterranean and the North East Atlantic, researches focused on different areas, complicating comparisons among studies. Murphy et al. (2006) studied the morphological variation of Delphinus delphis in the eastern North Atlantic and found a latitudinal cline in size, with northern mature males being slightly larger in mandible length, skull width and total body length compared to dolphins from the northwest coast of Spain. The Portuguese population showed segregation in morphometric characteristics (skull width in males and orbital measurements in females) suggesting the mixing of common dolphins off the Portuguese coast with common dolphins in the Mediterranean and farther south. Westgate (2007) analysed the cranial morphology of short-beaked common dolphins from the eastern and western North Atlantic and detected subtle but significant differences both in males and females, with rostral width as an important discriminating variable. The occipital region of the skull supports the separation of the Mediterranean common dolphins from the Irish, British and Danish populations (Nicolosi 2011). Distinct cranial features were detected in the coastal French and Mediterranean striped dolphins compared to the Scottish stocks (Loy et al. 2011). In this case, shape differences involved mainly the rostral and occipital regions of the skull. However, morphological variation of the bottlenose dolphin has little been investigated in this geographical area. De Francesco and Loy (2016) explored sexual dimorphism and ontogenetic allometry in the bottlenose dolphin T. truncatus living in mono- or interspecific associations in the Mediterranean and the North Sea, and found sexual dimorphic asymmetric traits in the North Sea dolphins living in monospecific associations, with females bearing a marked incision of the cavity hosting the left tympanic bulla. These differences were related to a more refined echolocalization system that likely enhances the exploitation of local resources by philopatric females.

Taking into account the evidences of both genetic and morphological segregation between the Mediterranean and the eastern North Atlantic populations observed in many cetacean taxa, and considering the specific conditions of the Mediterranean and the Atlantic environments, we here explored the mandibular morphology of D. delphis, T. truncatus and S. coeruleoalba to test the following hypotheses: (1) the three dolphin species exhibit significant differences in mandibular size and shape between the Mediterranean and the extra-Mediterranean stocks (2) morphological variation in the three species follows similar trajectories of size and shape changes across discrete geographic areas. Being deeply involved in both feeding adaptation and echolocation (Hanken and Hall 1993), we expect the morphology of the three dolphins’ mandible to converge under similar selective pressures across localities, and to reflect phylogenetic distances among species, especially to preserve specific communication skills across geography.

Materials and Methods

Data were collected on a total of 220 specimens belonging to Delphinus delphis (n = 64), Stenella coeruleoalba (n = 51) and T. truncatus (n = 104). Each species is represented by populations coming from three broad geographic areas: the Mediterranean Sea (MS), the North East Atlantic (AO) and the North Sea (NS) (Online Resources 1, 2, 3).

Only adult individuals, having more than 7 years old (Cagnolaro et al. 2015), were selected. When age information was not available, the shape of the coronoid crest and of the tip of the mandible was used a proxy of age: juveniles have a low and wide crest and a thin mandibular tip; as the animal matures, the crest forms a distinct and narrow ridge and the mandibular symphysis begins to thicken becoming blunt in older animals (Perrin 1975; Mead and Fordyce 2009). Mandibles were photographed in lateral view with a Nikon 3100 camera set at a fixed distance from the object (1.5 m). Eight landmarks (Fig. 1) were recorded to provide adequate coverage of the mandibular morphology.

Fig. 1
figure1

Location of landmarks on the right hemi-mandible. Landmark descriptions as follow: (1) Most anterior tip of the mandible; (2) Posterior ventral tip of the angular process; (3) Ventral extreme point of the condylar process; (4) Dorsal extreme point of the condylar process; (5) Most concave point of the mandibular notch; (6) Tip of the coronoid process; (7) Most posterior end of alveolar groove; (8) Most anterior end of alveolar groove

Landmarks were digitized on the right hemi-mandible using the software tpsDig2 version 2.26 (Rohlf 2003). We selected the right hemi-mandible because there were more undamaged specimens available. To measure the two nested sources of error associated with imaging and digitizing, ten specimens were photographed twice and, on each image, the eight-landmarks were digitized twice on two different days. A Procrustes analysis of variance (ANOVA) was run in MorphoJ version 1.06b to test for image and digitizing error (Klingenberg 2011, http://www.flywings.org.uk/MorphoJ_page.htm).

A generalized Procrustes analysis (GPA) was performed to translate, scale and rotate all landmark configurations in order to minimize the average distances of configurations from the reference. The reference in GPA is an iteratively computed mean configuration (Rohlf and Slice 1990). GPA removes all sources of variation that are not shape differences and separates shape from size. The size variable is the centroid size (CS), which is the square root of the summed squared distances of each landmark from the centroid of the landmark configuration. Shape variables are new coordinates that describe the location of each specimen in a curved space related to Kendall’s shape space and represent the difference between the consensus and each sample (Slice 2001). These differences are measured as Procrustes distances. Since most methods of multivariate statistics assume a Euclidean space, after superimposition shape coordinates are projected from Kendall’s space onto a Euclidean space tangent to the consensus. Multivariate analyses can be run in this tangent space in which linear distances among configurations approximate original Procrustes distances in Kendall’s space (Zelditch et al. 2012).

Shape and size differences were investigated: (i) at the intraspecific level, comparing different populations within each species, (ii) at the interspecific level, studying differences among the three species (pooling the three populations of each taxon), (iii) comparing populations by pooling different species coming from the same area. To assess shape and size differences between sexes (intraspecific variation) we performed a Procrustes ANOVA as implemented in the R package geomorph (Adams and Otárola-Castillo 2013) in R Studio version 0.98.1103 (R Studio) with 9999 iterations, using Procrustes distances and centroid size values respectively (D. delphis: f = 11, m = 21, unknown = 32; S. coeruleoalba: f = 18, m = 27, unknown = 6; T. truncatus: f = 36, m = 40, unknown = 28).

A one-way non-parametric multivariate analysis of variance (MANOVA) on Procrustes coordinates was run to test for significant differences among populations within each species (software PAST, version 2.17c, Hammer et al. 2001). When within a species all population pairs were different, a canonical variate analysis (CVA) was further conducted to identify the shape features that best distinguished the three geographical groups.

At the interspecific level, the Procrustes ANOVA was employed to test the null-hypothesis (H0) that there is no significant size and shape difference among species and populations.

To statistically compare patterns of phenotypic changes among species’ populations from the three selected geographic areas, we employed the function trajectory analysis (R package geomorph). Phenotypic change along a geographic gradient is represented by a trajectory connecting samples from three different seas along a latitudinal gradient (Collyer and Adams 2013; Meloro et al. 2014). The phenotypic trajectory analysis computes pairwise comparisons among the geometric attributes of the trajectories, describing the shape (S), the magnitude (D) and the orientation (Ѳ) of phenotypic changes. For each species, the differences in shape are computed as the deviations between corresponding geographical levels across two scaled and aligned phenotypic trajectories expressed as Euclidean distances. The magnitude is the path-length distance, derived from the sum of the Euclidean distances of sequential geographical levels within each trajectory and defines the amount of shape change; the orientation is the direction of its first principal component (PC1). When phenotypic change is quantified across two levels, the change is represented by a vector connecting the phenotypic means of the two levels. Compared to trajectories, vectors can be mathematically described by two attributes: magnitude and direction of phenotypic change. The trajectory and vector’s attributes are calculated for each species and then statistically compared to infer how patterns of phenotypic change diverge. The variation in attributes is assessed via permutation and the extent to which they are concordant allows to detect differences or similarities among patterns of phenotypic variation (Adams and Collyer 2009). Trajectories are visualized in the space of principal components (PC1 and PC2) and display the phenotypic change that occurs from one geographic region to another. For each pairwise comparison, attribute differences are significant if the P values from a generally high number of permutations (9999) are less than a type I error rate of α < 0.05. An analysis of variance (ANOVA) was performed with type I sums of squares (SS) and a randomized residual permutation procedure (RRPP) (Collyer et al. 2015).

The function procD.allometry (R package geomorph) was used first to investigate intraspecific allometry in each species, and then to test for significant interspecific differences among allometric trends with natural log-transformed centroid size (lnCS) as the covariate predictor. This was done by performing an ANOVA for homogeneity of slopes.

Results

Measurement Error

The Procrustes ANOVA run among distinct sampling replicates demonstrated that the shape variables and centroid size values obtained through each session of data acquisition were not significantly different. For both size (F = 114.09, P < 0.001) and shape (F = 173.05, P < 0.001), differences among individuals significantly accounted for 97% of total variation. Differences among replicates due to imaging were non-significant and explained about 0.7% while the digitalization error accounted for less than 1.7%.

Intraspecific Shape and Size Variation

In each species, sexual dimorphism was not significant neither in size nor shape (Table 1). The analyses provided no evidence of sexual dimorphism for the mandibular structure. Therefore, all subsequent analyses were conducted on pooled samples of both sexes, including the specimens of unknown sex.

Table 1 ANOVA based on a randomized residual permutation procedure (RRPP) with 1000 random permutations

In all three species, non-parametric MANOVA performed on Procrustes coordinates showed significant differences between populations (D. delphis: TSS (= total sum of squares) = 0.033, WSS (= within sum of squares) = 0.028, F = 6.138, P < 0.001; S. coeruleoalba: TSS = 0.022, WSS = 0.019, F = 3.064, P < 0.01; T. truncatus: TSS = 0.083, WSS = 0.075, F = 5.554, P < 0.001). As for D. delphis and S. coeruleoalba, post hoc tests revealed significant differences between all populations except when considering North Sea vs Atlantic Ocean (see Table 2). In the bottlenose dolphin, significant shape differences in all population pairs were detected (Table 2). The CVA plot (Fig. 2) displayed the discrimination among the three populations and highlighted the differentiation between the Mediterranean and the North Sea specimens. Wireframe graphs showed that morphological changes are concentrated in the ramus, which is wider, with more developed condylar and coronoid processes compared to the Mediterranean configuration.

Table 2 Pairwise comparisons among D. delphis, S. coeruleoalba and T. truncatus’ populations. Statistically significant comparisons are highlighted in bold
Fig. 2
figure2

Scatter plot of CV scores for the three populations of T. truncatus. Shape differences are displayed as wireframe graphs of deviations (dark blue) from the mean shape (light blue) at the extremes of the axis showing the higher separation among the seas. Scale factor = 8. (Color figure online)

Interspecific Size and Shape Variation

Size

An ANOVA test with permutations was run to test for significant interspecific differences among means and then a multiple comparison test among species was conducted. Size was significantly different among taxa (F = 57.987, df = 2, P value < 0.01) (Fig. 3) and populations (F = 14.140, df = 2, P value < 0.01) but after pairwise comparisons, the bottlenose dolphin was the only significantly different species with respect to the other small dolphins (P value < 0.001). A more complex model including both species and populations as factors detected a significant interaction between the two independent variables (F = 4.664, df = 4, P value < 0.01).

Fig. 3
figure3

Box plot for centroid size (CS) for the three species. Dd Delphinus delphis, Sc Stenella coeruleoalba, Tt Tursiops truncatus. The level of significance for each pairwise comparison is indicated by stars on significance bars: ***P < 0.001; NS Not significant

Shape

The first two PCs extracted from shape variables accounted for 75% of total variation (Fig. 4). Species were best discriminated along the first axis (63% of variance), with the bottlenose dolphin clearly separated in correspondence of the positive scores. Shape changes along the first PC concern the alveolar groove’s length and the ramus’ expansion that are inversely correlated: on the negative scores, the common dolphin and the striped dolphin show a narrow jaw morphology characterized by a longer tooth row and a reduced ramus width, whereas the bottlenose dolphin has a massive mandible with a shorter dental groove and a wider ramus, distinctly developed along the dorso-ventral axis. The Procrustes ANOVA highlighted significant interspecific differences among species and populations together with the interaction between the two factors (Table 3).

Fig. 4
figure4

Shape variation of Delphinus delphis (red) Stenella coeruleoalba (green) and Tursiops truncatus (blue) along the first two principal components axes, summarizing 75% of cumulative variance. Wireframe graphs for the extremes of the first axis are shown, light blue line refers to the reference configuration, dark blue line represents the configuration corresponding to the extreme of the axis. Scale factor = 0.1. (Color figure online)

Table 3 ANOVA based on a randomized residual permutation procedure (RRPP) with 1000 random permutations

We analysed phenotypic trajectory changes in the three species along the geographic gradient from the Mediterranean to the North Sea (Fig. 5; Table 4), including the three areas under study: the Mediterranean Sea, the North-East Atlantic and the North Sea. The analysis evidenced that the three species display similar magnitudes and directions of phenotypic changes (Table 4).

Fig. 5
figure5

Left: geographic trajectories for the three species D. delphis (Dd, red) S. coeruleoalba (Sc, green) and T. truncatus (Tt, blue) across three geographical areas: white, grey and black points represent respectively the mean shape for the Mediterranean Sea, the North East Atlantic Ocean and the North Sea. Right: geographic vectors for the three species D. delphis (Dd, red) S. coeruleoalba (Sc, green) and T. truncatus (Tt, blue) across two geographical areas: white, and black points represent respectively the mean shape for the Mediterranean Sea and the North Atlantic Ocean. Trajectories and vectors are displayed along the first two principal component axes summarizing 75% of cumulative variance. (Color figure online)

Table 4 Pairwise comparisons of geometric attributes of phenotypic trajectories for each species across the three geographic areas

Each taxon exhibits the same amount of phenotypic change along the trajectory from the Mediterranean to the North East Atlantic. In the striped dolphin, shape changes are mainly expressed along the second PC, while for the common and the bottlenose dolphin, shape variation is distributed along the first PC (Fig. 5). The magnitude of shape changes is similar among species except for the common dolphin which shows a shorter path (Table 4).

Since most pairwise comparisons did not show any significant difference between the North East Atlantic and the North Sea populations, a phenotypic change vector (PCV) method (Adams and Collyer 2009) was used combining these two in a single population (extra-Mediterranean). An ANOVA performed on the Procrustes distances detected significant differences among Species, Seas and their interaction (Table 5).

Table 5 ANOVA based on a randomized residual permutation procedure (RRPP) with 1000 random permutations

The analysis of phenotypic vectors between the Mediterranean Sea and the extra Mediterranean showed the same low and non-significant amount of shape change among the three taxa (DD, S = 0.001, P = 0.745; DD, T = 0.002, P = 0.490; DS, T = 0.001, P = 0.770), while the direction of phenotypic change was significantly different between the bottlenose dolphin and the other two species (ѲD, T = 75.730°, P = 0.015; Ѳ S, T = 99.681°, P = 0.005). The angle between the striped and the common dolphin was not significantly different from random expectation even if it was particularly large (Ѳ D, S = 71.177°, P = 0.070).

Figure 6 compares species’ shape configurations corresponding to the two geographic areas as deformation grids associated to the population mean on PC1 and PC2: the Mediterranean Sea and the North Atlantic Ocean. The Mediterranean common dolphins have a longer corpus with a thinner mandibular tip and a smaller ramus compared to the Atlantic stock. Morphological variation is concentrated on landmarks corresponding to the end of the alveolar line and to the angular and coronoid processes. Striped dolphin’s shape changes involve the position of the angular and the condylar processes. In the Atlantic group, specimens display a more robust mandible with the angular process that expands posteriorly, and a shorter corpus expanded along the dorso-ventral axis. In the Mediterranean population, the angular process moves anteriorly and the ramus profile is more rounded. The bottlenose dolphin shows different morphological shape changes across the geographical gradient compared to the other two species. Unlike the Mediterranean specimens, the Atlantic population has a shorter corpus and a wider ramus which is characterized by an expansion of the condylar process along the antero-posterior axis and the coronoid and angular processes developed along the dorso-ventral one.

Fig. 6
figure6

Deformation grids, produced with TpsRelw, show features of mean shape configurations corresponding to the Mediterranean and extra-Mediterranean populations of the three species along PC1 (dark blue line), compared to the mean configuration of each species calculated on PC1 and PC2 scores. Scale factor = 5. (Color figure online)

Allometry

A significant association was detected between size (lnCS) and shape in the whole sample with size explaining 19% of the total shape variation (df = 1; SS = 0.053; MS = 0.053; R2 = 0.193; F = 87.497; Z = 21.929; P < 0.01). The null hypothesis of parallel slopes among species was rejected based on a significance criterion of alpha = 0.05 (group allometries: df = 210; SSE = 0.124; SS = 0.004; R2 = 0.017; F = 3.748; Z = 2.992; P < 0.05). Figure 7 shows allometric trajectories as the first principal component of predicted shape values on lnCS (Adams and Nistri 2010; Adams et al. 2013).

Fig. 7
figure7

Allometric trajectories are shown as the first principal component of predicted shape values on log-transformed centroid size (lnCS). Green, red and black dots represent respectively Tursiops truncatus, Stenella coeruleoalba and Delphinus delphis. (Color figure online)

In the bottlenose dolphin, CS accounted for 9% of the total shape variation (1000 permutation runs, P < 0.001) while in the common and the striped dolphins the effect of size on shape was not significant (1000 permutation runs, D. delphis: P = 0.209, S. coeruleoalba: P = 0.066).

Discussion

Mandibular size and shape vary significantly between small cetacean species and we demonstrated that they allow to identify ecogeographical patterns in these aquatic mammals. According to previous analyses (Guidarelli et al. 2014), we observed a clear discrimination of the bottlenose dolphin from the striped and common dolphin. The greater similarity between the two small dolphins compared to the bottlenose dolphin supports phylogenies based on molecular data (Amaral et al. 2007, 2012) that suggest a closer phylogenetic relationship between the striped and common dolphins. T. truncatus’ mandible is large and massive with a shorter alveolar groove while S. coeruleoalba and D. delphis are characterized by a slender and longer tooth row (Fig. 4).

At the intraspecific level, significant shape differences occur between the Mediterranean populations and the extra-Mediterranean ones, whereas differences of smaller magnitude were found between the Northeast Atlantic and the North Sea stocks of dolphins. The only exception concerns the striped dolphin, whose Mediterranean population is significantly different from the North Sea but not from the North East Atlantic stock. Loy et al. (2011) already identified similarities in the cranium shape of North-East Atlantic striped dolphins and the Mediterranean ones, reinforcing our lack of significant differentiation in the mandible. The CVA performed on the largest sample of T. truncatus, showed that the extra-Mediterranean population displays an extended ramus with pronounced condylar and coronoid processes and a wide coronoid crest. The Mediterranean one has a relatively slender morphology with a restricted ramus and a thinner mandibular symphysis (Figs. 2, 6). Such changes cannot be identified in the two small delphinids (Fig. 6), supporting a profound ecomorphological differentiation of the bottlenose dolphin from the other species. T. truncatus differs in size, allometric trajectory and direction of shape change vectors while, on the other hand, the striped and common dolphins share similar mandibular size values, the same direction of shape change and allometric trajectories. Striped and common dolphins from the extra-Mediterranean area have a similar morphology defined by an expanded angular process along the antero–posterior axis and a slender shape compared to the bottlenose dolphin (Fig. 6). As for the Mediterranean populations, the mandible has a restricted angular process and a well-pronounced mandibular notch. However, when the two geographic areas are compared, the two small dolphins seem to diverge in the Mediterranean Sea and to converge outside of this basin.

Differences in feeding apparatus morphologies and diets revealed in both terrestrial (Adams and Rohlf 2000) and marine vertebrates (del Castillo et al. 2017) may indicate how partitioning of ecological niches reduce the occurrence of competition for food resources when the species are in direct sympatry (Bearzi 2005). Many studies have demonstrated that the mandible exhibits a strong correlation between form and diet, showing how adaptation to different feeding strategies and food consistency can rapidly shape the mandibular structure (Anderson et al. 2014; Meloro 2011; Meloro and O’Higgins 2011; Raia et al. 2010; Raia 2004). Therefore, mandibular shape changes could be explained in terms of adaptive processes (resulting in convergence or divergence) related to interspecific interactions and feeding ecology. The common dolphin is mainly considered a neritic predator feeding on epipelagic and mesopelagic shoaling fish (e.g., anchovies Engraulidae, sardines Sardina pilchardus) in both the Mediterranean Sea and the Atlantic Ocean (Bearzi et al. 2003; Spitz et al. 2006a; Silva 1999). However, even when living in the oceanic domain, the common dolphin seems to select a particular prey type, which is small shoaling migrating mesopelagic fish, rather than a particular prey species (Pusineri et al. 2007). In the Mediterranean Sea, D. delphis is often observed in association with S. coeruleoalba (Bearzi et al. 2003) with a decreasing eastward gradient of relative abundance of common dolphins likely relative to its capacity to form single species group: as the number of common dolphins decreases, their groups start to depend on striped dolphins and move to mixed groups (Frantzis and Herzing 2002). No evidence of food competition exists between the two species because contrarily to the common dolphin, the Mediterranean diet of the striped dolphin is mainly based on demersal (Lahaye et al. 2006) and pelagic cephalopods (e.g. Ommastrephidae, Histioteuthidae, Onychoteuthidae) (Wurtz and Marrale 1993; Meotti and Podestà 1997). The taller shape of the striped dolphin’s ramus observed in the Mediterranean stock is concordant with its teuthophagous diet since from an evolutionary point of view, more robust mandibles are correlated with a suction feeding strategy rather than a raptorial behaviour (Johnston and Berta 2011; Werth 2000). Outside the basin, the striped dolphin is mainly observed in oceanic waters feeding primarily on small mesopelagic fish (Spitz et al. 2006b; Pusineri et al. 2007) whereas the common dolphin lives in neritic areas occurring mostly over the continental shelf (Silva 1999), likely limiting the interspecific competition for food resources.

The bottlenose dolphin shows a clearly different pattern of shape change across the geographic gradient compared with the other two dolphins (Fig. 6; Table 4). Because its allometric component is significant, T. truncatus’ shape changes are clearly related to size variation. The Atlantic population’s jaw morphology is more robust compared to the Mediterranean one and is characterized by well-developed bony processes and a prominent mandibular notch, possibly reflecting muscle insertion for a stronger musculature (Mead and Fordyce 2009). The species is generally considered an opportunistic feeder and a top predator of coastal and shelf habitats. However, in the Mediterranean its diet is primarily based on demersal prey such as the European hake Merluccius merluccius, European conger Conger conger, common cuttlefish Sepia officinalis, common octopus Octopus vulgaris (Blanco et al. 2001; Bearzi et al. 2009). The importance of hakes in the Mediterranean diet contrasts with the greater importance of gadids (e.g., whiting Merlangius merlangius) in the East Atlantic (Santos et al. 1994; Blanco et al. 2001) and with a diet inclusive of big preys such as haddock Melanogrammus aeglefinus and large salmonids, Salmo salar and Salmo trutta, in northern latitudes including the Black Sea (Wilson et al. 1997; Santos 1998; Santos et al. 2001).

Despite a high level of sympatry with the common dolphin in the Mediterranean neritic habitat, associations between the two species have rarely been observed (Bearzi et al. 2005). Whether this could be related to different prey preferences is not known, however remarkably different feeding strategies have been observed: the bottlenose dolphin performs long dives (up to 8 min) preying on demersal species while the common dolphin performs shorter dives (less than 2 min) and prefers small epipelagic fishes. Our morphological data supports this dietary segregation since D. delphis’ slender mandibular shape is typically related to the raptorial feeding strategy while T. truncatus’ blunted jaw (i.e., shorter length, higher ramus and reduced dentition) corresponds to a suction feeder structure.

Finally, despite the observed differences between the bottlenose dolphin mandibular morphology and the other two small species, it is worth noting that they display some common patterns of geographic phenotypic change: first, the Mediterranean populations are always clearly different from the Atlantic ones; second, the amount of phenotypic change is significantly similar among species. From an evolutionary point of view, after the isolation of the Mediterranean Basin during the Messinian salinity crisis, which occurred in the late Miocene (5.59–5.33 Ma) (Krijgsman et al. 1999), the Atlantic waters rapidly refilled the basin (Garcia-Castellanos et al. 2009). In fact, while the Italian Miocene fossil record is almost negligible, the Italian Pliocene fossils testify to the Mediterranean’s colonization by the Atlantic oceanic fauna (Cagnolaro et al. 2015). Sharing the same semi-enclosed basin could have led to a more pronounced interspecific niche segregation within the basin compared to the Atlantic Ocean, with species displaying habitat partitioning to avoid direct competition. Here, the mandibular structural divergence observed in the Mediterranean stocks of the striped and the common dolphins seems to support this hypothesis while, on the other hand, the Mediterranean morphological divergence of the bottlenose dolphin could be related to the marked difference of prey type (e.g., lack of big and large prey living in northern latitudes). Future research should concentrate on these aspects of evolutionary ecology to link the observed anatomical differences to different functional demands related to distinct diet preferences. Last but not least, we underline the role of geometric morphometrics to investigate the morphological variability of species both at the intraspecific and interspecific level and to identify functional important anatomical changes.

This research received financial support from the University of Molise and through SYNTHESYS funding (Grant Agreement No 226506) within the European Union’s Seventh Framework Programme.

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Acknowledgements

The authors warmly thank the curators of the following institutions for providing access to the collections and to museum facilities: Museo Civico di Storia Naturale, Milano; Museo Civico di Storia Naturale “G. Doria”, Genova; Museo Civico di Zoologia, Roma; Museo di Storia Naturale, Calci; Museo Zoologico, Università di Firenze; Accademia dei Fisiocritici di Siena; Muséum National d’Histoire Naturelle, Paris; Naturalis Biodiversity Center, Leiden; Royal Belgian Institute of Natural Sciences, Bruxelles; Zoological Museum, University of Copenhagen; National History Museum of Scotland, Edinburgh; University of Haifa, Israel; Natural History Museum, Tel Aviv University; Aquário Vasco da Gama, Lisboa; Museu Nacional de História Natural e da Ciência, Lisboa; Naturhistoriska riksmuseet, Stockholm; Zoological Museum, Barcelona. This research received financial support from the University of Molise and through SYNTHESYS funding (Grant Agreement No. 226506) within the European Union’s Seventh Framework Programme.

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Correspondence to Giulia Guidarelli or Carlo Meloro.

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Guidarelli, G., Colangelo, P., de Francesco, M.C. et al. Phenotypic Changes Across a Geographic Gradient: The Case of Three Sympatric Dolphin Species. Evol Biol 45, 113–125 (2018). https://doi.org/10.1007/s11692-017-9435-6

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Keywords

  • Geometric morphometrics
  • Mandible
  • Stenella coeruleoalba
  • Tursiops truncatus
  • Delphinus delphis
  • Phenotypic change vectors