Dataset Information

Evolution of a complex phenotype with biphasic ontogeny: Contribution of development versus function and climatic variation to skull modularity in toads.

ABSTRACT: The theory of morphological integration and modularity predicts that if functional correlations among traits are relevant to mean population fitness, the genetic basis of development will be molded by stabilizing selection to match functional patterns. Yet, how much functional interactions actually shape the fitness landscape is still an open question. We used the anuran skull as a model of a complex phenotype for which we can separate developmental and functional modularity. We hypothesized that functional modularity associated to functional demands of the adult skull would overcome developmental modularity associated to bone origin at the larval phase because metamorphosis would erase the developmental signal. We tested this hypothesis in toad species of the Rhinella granulosa complex using species phenotypic correlation pattern (P-matrices). Given that the toad species are distributed in very distinct habitats and the skull has important functions related to climatic conditions, we also hypothesized that differences in skull trait covariance pattern are associated to differences in climatic variables among species. Functional and hormonal-regulated modules are more conspicuous than developmental modules only when size variation is retained on species P-matrices. Without size variation, there is a clear modularity signal of developmental units, but most species have the functional model as the best supported by empirical data without allometric size variation. Closely related toad species have more similar climatic niches and P-matrices than distantly related species, suggesting phylogenetic niche conservatism. We infer that the modularity signal due to embryonic origin of bones, which happens early in ontogeny, is blurred by the process of growth that occurs later in ontogeny. We suggest that the species differing in the preferred modularity model have different demands on the orbital functional unit and that species contrasting in climate are subjected to divergent patterns of natural selection associated to neurocranial allometry and T3 hormone regulation.

SUBMITTER: Simon MN

PROVIDER: S-EPMC5743631 | biostudies-literature | 2017 Dec

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Evolution of a complex phenotype with biphasic ontogeny: Contribution of development versus function and climatic variation to skull modularity in toads.

Simon Monique Nouailhetas MN Marroig Gabriel G

Ecology and evolution 20171107 24

The theory of morphological integration and modularity predicts that if functional correlations among traits are relevant to mean population fitness, the genetic basis of development will be molded by stabilizing selection to match functional patterns. Yet, how much functional interactions actually shape the fitness landscape is still an open question. We used the anuran skull as a model of a complex phenotype for which we can separate developmental and functional modularity. We hypothesized tha ...[more]

PMID: 29299255

Similar Datasets

Project description:BackgroundCaecilians (Gymnophiona) are the least speciose extant lissamphibian order, yet living forms capture approximately 250 million years of evolution since their earliest divergences. This long history is reflected in the broad range of skull morphologies exhibited by this largely fossorial, but developmentally diverse, clade. However, this diversity of form makes quantification of caecilian cranial morphology challenging, with highly variable presence or absence of many structures. Consequently, few studies have examined morphological evolution across caecilians. This extensive variation also raises the question of degree of conservation of cranial modules (semi-autonomous subsets of highly-integrated traits) within this clade, allowing us to assess the importance of modular organisation in shaping morphological evolution. We used an intensive surface geometric morphometric approach to quantify cranial morphological variation across all 32 extant caecilian genera. We defined 16 cranial regions using 53 landmarks and 687 curve and 729 surface sliding semilandmarks. With these unprecedented high-dimensional data, we analysed cranial shape and modularity across caecilians assessing phylogenetic, allometric and ecological influences on cranial evolution, as well as investigating the relationships among integration, evolutionary rate, and morphological disparity.ResultsWe found highest support for a ten-module model, with greater integration of the posterior skull. Phylogenetic signal was significant (Kmult?=?0.87, p < 0.01), but stronger in anterior modules, while allometric influences were also significant (R2?=?0.16, p?< 0.01), but stronger posteriorly. Reproductive strategy and degree of fossoriality were small but significant influences on cranial morphology (R2?=?0.03-0.05), after phylogenetic (p?<?0.03) and multiple-test (p?<?0.05) corrections. The quadrate-squamosal 'cheek' module was the fastest evolving module, perhaps due to its pivotal role in the unique dual jaw-closing mechanism of caecilians. Highly integrated modules exhibited both high and low disparities, and no relationship was evident between integration and evolutionary rate.ConclusionsOur high-dimensional approach robustly characterises caecilian cranial evolution and demonstrates that caecilian crania are highly modular and that cranial modules are shaped by differential phylogenetic, allometric, and ecological effects. More broadly, and in contrast to recent studies, this work suggests that there is no simple relationship between integration and evolutionary rate or disparity.

Project description:BackgroundThe skull of placental mammals constitutes one of the best studied systems for phenotypic modularity. Several studies have found strong evidence for the conserved presence of two- and six-module architectures, while the strength of trait correlations (integration) has been associated with major developmental processes such as somatic growth, muscle-bone interactions, and tooth eruption. Among placentals, ant- and termite-eating (myrmecophagy) represents an exemplar case of dietary convergence, accompanied by the selection of several cranial morphofunctional traits such as rostrum elongation, tooth loss, and mastication loss. Despite such drastic functional modifications, the covariance patterns of the skull of convergently evolved myrmecophagous placentals are yet to be studied in order to assess the potential consequences of this dietary shift on cranial modularity.ResultsHere, we performed a landmark-based morphometric analysis of cranial covariance patterns in 13 species of myrmecophagous placentals. Our analyses reveal that most myrmecophagous species present skulls divided into six to seven modules (depending on the confirmatory method used), with architectures similar to those of non-myrmecophagous placentals (therian six modules). Within-module integration is also similar to what was previously described for other placentals, suggesting that most covariance-generating processes are conserved across the clade. Nevertheless, we show that extreme rostrum elongation and tooth loss in myrmecophagid anteaters have resulted in a shift in intermodule correlations in the proximal region of the rostrum. Namely, the naso-frontal and maxillo-palatine regions are strongly correlated with the oro-nasal module, suggesting an integrated rostrum conserved from pre-natal developmental processes. In contrast, the similarly toothless pangolins show a weaker correlation between the anterior rostral modules, resembling the pattern of toothed placentals.ConclusionsThese results reveal that despite some integration shifts related to extreme functional and morphological features of myrmecophagous skulls, cranial modular architectures have conserved the typical mammalian scheme.

Project description:BackgroundIn amphibians, thyroid hormone (TH) has a profound role in cranial development, especially in ossification of the late-appearing bones and remodeling of the skull. In the present study, we explored the influence of TH deficiency on bone ossification and resulting skull shape during the ontogeny of Triturus newt hybrid larvae obtained from interspecific crosses between T. ivanbureschi and T. macedonicus.MethodsLarvae were treated with two concentrations of thiourea (an endocrine disruptor that chemically inhibits synthesis of TH) during the midlarval and late larval periods. Morphological differences of the cranium were assessed at the end of the midlarval period (ontogenetic stage 62) and the metamorphic stage after treatment during the late larval period.ResultsThere was no difference in the ossification level and shape of the skull between the experimental groups (control and two treatment concentrations) at stage 62. During the late larval period and metamorphosis, TH deficit had a significant impact on the level of bone ossification and skull shape with no differences between the two treatment concentrations of thiourea. The most pronounced differences in bone development were: the palatopterygoid failed to disintegrate into the palatal and pterygoid portions, retardation was observed in development of the maxilla, nasal and prefrontal bones and larval organization of the vomer was retained in thiourea-treated larvae.ConclusionsThis implies that deficiency of TH caused retardation in development and arrested metamorphic cranium skeletal reorganization, which resulted in divergent cranial shape compared to the control group. Our results confirmed that skull remodeling and ossification of late-appearing bones is TH-dependent, as in other studied Urodela species. Also, our results indicate that TH plays an important role in the establishment of skull shape during the ontogeny of Triturus newts, especially during the late larval period and metamorphosis, when TH concentrations reach their maximum.

Dataset Information

Evolution of a complex phenotype with biphasic ontogeny: Contribution of development versus function and climatic variation to skull modularity in toads.

Publications

Evolution of a complex phenotype with biphasic ontogeny: Contribution of development versus function and climatic variation to skull modularity in toads.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets