Selection and Constraints in the Ecomorphological Adaptive Evolution of the Skull of Living Canidae (Carnivora, Mammalia).

The association between phenotype and ecology is essential for understanding the environmental drivers of morphological evolution. This is a particularly challenging task when dealing with complex traits, such as the skull, where multiple selective pressures are at play and evolution might be constrained by ontogenetic and genetic factors. I integrate morphometric tools, comparative methods, and quantitative genetics to investigate how ontogenetic constraints and selection might have interacted during the evolution of the skull in extant Canidae. The results confirm that the evolution of cranial morphology was largely adaptive and molded by changes in diet composition. While the investigation of the adaptive landscape reveals two main selective lines of least resistance (one associated with size and one associated with functional shape features), rates of evolution along size were higher than those found for shape dimensions, suggesting the influence of constraints on morphological evolution. Structural modeling analyses revealed that size, which is the line of most genetic/phenotypic variation, might have acted as a constraint, negatively impacting dietary evolution. Constraints might have been overcome in the case of selection for the consumption of large prey by associating strong selection along both size and shape directions. The results obtained here show that microevolutionary constraints may have played a role in shaping macroevolutionary patterns of morphological evolution.

Evolution of morphological integration in the skull of Carnivora (Mammalia): Changes in Canidae lead to increased evolutionary potential of facial traits.

Morphological integration refers to the fact that different phenotypic traits of organisms are not fully independent from each other, and tend to covary to different degrees. The covariation among traits is thought to reflect properties of the species' genetic architecture and thus can have an impact on evolutionary responses. Furthermore, if morphological integration changes along the history of a group, inferences of past selection regimes might be problematic. Here, we evaluated the stability and evolution of the morphological integration of skull traits in Carnivora by using evolutionary simulations and phylogenetic comparative methods. Our results show that carnivoran species are able to respond to natural selection in a very similar way. Our comparative analyses show that the phylogenetic signal for pattern of integration is lower than that observed for morphology (trait averages), and that integration was stable throughout the evolution of the group. That notwithstanding, Canidae differed from other families by having higher integration, evolvability, flexibility, and allometric coefficients on the facial region. These changes might have allowed canids to rapidly adapt to different food sources, helping to explain not only the phenotypic diversification of the family, but also why humans were able to generate such a great diversity of dog breeds through artificial selection.

Aquatic adaptations in a Neotropical coral snake: a study of morphological convergence

Micrurus surinamensis is an aquatic member of the genus Micrurus. This species is known for its highly specialized venom and distinctive diet, mostly made of aquatic vertebrates. Here, we explore both external (head and body) and skull shape morphologies in M.surinamensis, comparing it with two terrestrial species of the genus (M.lemniscatus and M.spixii) and to aquatic and terrestrial species of distantly related groups. We use both traditional and geometric morphometrics to determine whether the presence of similar traits in head shape morphology is rather the result of adaptive convergences between M.surinamensis and other aquatic species, or whether it is the product of phylogenetic conservatism within the genus. Results from both traditional and geometric morphometrics show that M.surinamensis can be considered convergent with aquatic species, mainly in the skull shape. Micrurus surinamensis differs from the two terrestrial species of Micrurus by having a wider head, smaller distance between nostrils, and a long tail. Geometric morphometric analysis shows that despite having an extremely conserved skull and mandible shape, M.surinamensis shows a longer supratemporal and quadrate bones than in terrestrial Micrurus, indicating a larger gape for this species. A more kinetic skull combined with a larger gape would allow M.surinamensis to feed on fish, which represent larger and wider prey that contrast with the elongate prey, which compose the main diet of species in the genus Micrurus. Our results illustrate the importance of both phylogenetic conservatism and adaptation in shaping species morphology.

Aquatic adaptations in a Neotropical coral snake: a study of morphological convergence

Micrurus surinamensis is an aquatic member of the genus Micrurus. This species is known for its highly specialized venom and distinctive diet, mostly made of aquatic vertebrates. Here, we explore both external (head and body) and skull shape morphologies in M.surinamensis, comparing it with two terrestrial species of the genus (M.lemniscatus and M.spixii) and to aquatic and terrestrial species of distantly related groups. We use both traditional and geometric morphometrics to determine whether the presence of similar traits in head shape morphology is rather the result of adaptive convergences between M.surinamensis and other aquatic species, or whether it is the product of phylogenetic conservatism within the genus. Results from both traditional and geometric morphometrics show that M.surinamensis can be considered convergent with aquatic species, mainly in the skull shape. Micrurus surinamensis differs from the two terrestrial species of Micrurus by having a wider head, smaller distance between nostrils, and a long tail. Geometric morphometric analysis shows that despite having an extremely conserved skull and mandible shape, M.surinamensis shows a longer supratemporal and quadrate bones than in terrestrial Micrurus, indicating a larger gape for this species. A more kinetic skull combined with a larger gape would allow M.surinamensis to feed on fish, which represent larger and wider prey that contrast with the elongate prey, which compose the main diet of species in the genus Micrurus. Our results illustrate the importance of both phylogenetic conservatism and adaptation in shaping species morphology.

Cranial adaptations for feeding on snails in species of Sibynomorphus (Dipsadidae: Dipsadinae).

Neotropical "goo-eating" dipsadine snakes display a set of morphological and histo-chemical adaptations linked to the capture of their soft-bodied, viscous invertebrate prey. Within this group, species from the genus Sibynomorphus feed chiefly on snails and slugs. Here, we analyzed a series of skull and mandible characters in S. mikanii, S. neuwiedi and S. turgidus using geometric morphometrics, with the aim of assessing morphological adaptations related to slug- and snail-feeding in that genus. We further compared the results with Leptodeira annulata, a species that feeds on vertebrates. To evaluate shape differences of the skull and mandible between species we performed a multivariate analysis of variance and a linear discriminant analysis. Our results show that the narrow, elongate skull in S. mikanii may help with slug ingestion, while asymmetry in teeth number and mandibular shape in S. neuwiedi and S. turgidus are likely related to snail feeding.

Cranial adaptations for feeding on snails in species of Sibynomorphus (Dipsadidae: Dipsadinae)

Neotropical "goo-eating" dipsadine snakes display a set of morphological and histo-chemical adaptations linked to the capture of their soft-bodied, viscous invertebrate prey. Within this group, species from the genus Sibynomorphus feed chiefly on snails and slugs. Here, we analyzed a series of skull and mandible characters in S. mikanii, S. neuwiedi and S. turgidus using geometric morphometrics, with the aim of assessing morphological adaptations related to slug- and snail-feeding in that genus. We further compared the results with Leptodeira annulata, a species that feeds on vertebrates. To evaluate shape differences of the skull and mandible between species we performed a multivariate analysis of variance and a linear discriminant analysis. Our results show that the narrow, elongate skull in S. mikanii may help with slug ingestion, while asymmetry in teeth number and mandibular shape in S. neuwiedi and S. turgidus are likely related to snail feeding.

High evolutionary constraints limited adaptive responses to past climate changes in toad skulls.

Interactions among traits that build a complex structure may be represented as genetic covariation and correlation. Genetic correlations may act as constraints, deflecting the evolutionary response from the direction of natural selection. We investigated the relative importance of drift, selection, and constraints in driving skull divergence in a group of related toad species. The distributional range of these species encompasses very distinct habitats with important climatic differences and the species are primarily distinguished by differences in their skulls. Some parts of the toad skull, such as the snout, may have functional relevance in reproductive ecology, detecting water cues. Thus, we hypothesized that the species skull divergence was driven by natural selection associated with climatic variation. However, given that all species present high correlations among skull traits, our second prediction was of high constraints deflecting the response to selection. We first extracted the main morphological direction that is expected to be subjected to selection by using within- and between-species covariance matrices. We then used evolutionary regressions to investigate whether divergence along this direction is explained by climatic variation between species. We also used quantitative genetics models to test for a role of random drift versus natural selection in skull divergence and to reconstruct selection gradients along species phylogeny. Climatic variables explained high proportions of between-species variation in the most selected axis. However, most evolutionary responses were not in the direction of selection, but aligned with the direction of allometric size, the dimension of highest phenotypic variance in the ancestral population. We conclude that toad species have responded to selection related to climate in their skulls, yet high evolutionary constraints dominated species divergence and may limit species responses to future climate change.