A GWAS in Latin Americans identifies novel face shape loci, implicating VPS13B and a Denisovan introgressed region in facial variation.

To characterize the genetic basis of facial features in Latin Americans, we performed a genome-wide association study (GWAS) of more than 6000 individuals using 59 landmark-based measurements from two-dimensional profile photographs and ~9,000,000 genotyped or imputed single-nucleotide polymorphisms. We detected significant association of 32 traits with at least 1 (and up to 6) of 32 different genomic regions, more than doubling the number of robustly associated face morphology loci reported until now (from 11 to 23). These GWAS hits are strongly enriched in regulatory sequences active specifically during craniofacial development. The associated region in 1p12 includes a tract of archaic adaptive introgression, with a Denisovan haplotype common in Native Americans affecting particularly lip thickness. Among the nine previously unidentified face morphology loci we identified is the VPS13B gene region, and we show that variants in this region also affect midfacial morphology in mice.

Morphological evolution of the carnivoran sacrum.

The sacrum is a key piece of the vertebrate skeleton, since it connects the caudal region with the presacral region of the vertebral column and the hind limbs through the pelvis. Therefore, understanding its form and function is of great relevance in vertebrate ecomorphology. However, it is striking that morphometric studies that quantify its morphological evolution in relation to function are scarce. The main goal of this study is to investigate the morphological evolution of the sacrum in relation to its function in the mammalian order Carnivora, using three-dimensional (3D) geometric morphometrics. Principal component analysis under a phylogenetic background indicated that changes in sacrum morphology are mainly focused on the joint areas where it articulates with other parts of the skeleton allowing resistance to stress at these joints caused by increasing muscle loadings. In addition, we demonstrated that sacrum morphology is related to both the length of the tail relativised to the length of the body, and the length of the body relativised to body mass. We conclude that the sacrum in carnivores has evolved in response to the locomotor requirements of the species analysed, but in locomotion, each family has followed alternative morphological solutions to address the same functional demands.

Correction to 'Limited thermal plasticity and geographical divergence in the ovipositor of Drosophila suzukii'.

[This corrects the article DOI: 10.1098/rsos.191577.].

Drosophila suzukii wing spot size is robust to developmental temperature.

Phenotypic plasticity is an important mechanism allowing adaptation to new environments and as such it has been suggested to facilitate biological invasions. Under this assumption, invasive populations are predicted to exhibit stronger plastic responses than native populations. Drosophila suzukii is an invasive species whose males harbor a spot on the wing tip. In this study, by manipulating developmental temperature, we compare the phenotypic plasticity of wing spot size of two invasive populations with that of a native population. We then compare the results with data obtained from wild-caught flies from different natural populations. While both wing size and spot size are plastic to temperature, no difference in plasticity was detected between native and invasive populations, rejecting the hypothesis of a role of the wing-spot plasticity in the invasion success. In contrast, we observed a remarkable stability in the spot-to-wing ratio across temperatures, as well as among geographic populations. This stability suggests either that the spot relative size is under stabilizing selection, or that its variation might be constrained by a tight developmental correlation between spot size and wing size. Our data show that this correlation was lost at high temperature, leading to an increased variation in the relative spot size, particularly marked in the two invasive populations. This suggests: (a) that D. suzukii's development is impaired by hot temperatures, in agreement with the cold-adapted status of this species; (b) that the spot size can be decoupled from wing size, rejecting the hypothesis of an absolute constraint and suggesting that the wing color pattern might be under stabilizing (sexual) selection; and (c) that such sexual selection might be relaxed in the invasive populations. Finally, a subtle but consistent directional asymmetry in spot size was detected in favor of the right side in all populations and temperatures, possibly indicative of a lateralized sexual behavior.

Limited thermal plasticity and geographical divergence in the ovipositor of Drosophila suzukii.

Phenotypic plasticity has been repeatedly suggested to facilitate adaptation to new environmental conditions, as in invasions. Here, we investigate this possibility by focusing on the worldwide invasion of Drosophila suzukii: an invasive species that has rapidly colonized all continents over the last decade. This species is characterized by a highly developed ovipositor, allowing females to lay eggs through the skin of ripe fruits. Using a novel approach based on the combined use of scanning electron microscopy and photogrammetry, we quantified the ovipositor size and three-dimensional shape, contrasting invasive and native populations raised at three different developmental temperatures. We found a small but significant effect of temperature and geographical origin on the ovipositor shape, showing the occurrence of both geographical differentiation and plasticity to temperature. The shape reaction norms are in turn strikingly similar among populations, suggesting very little difference in shape plasticity among invasive and native populations, and therefore rejecting the hypothesis of a particular role for the plasticity of the ovipositor in the invasion success. Overall, the ovipositor shape seems to be a fairly robust trait, indicative of stabilizing selection. The large performance spectrum rather than the flexibility of the ovipositor would thus contribute to the success of D. suzukii worldwide invasion.

Estimating Phylogenies from Shape and Similar Multidimensional Data: Why It Is Not Reliable.

In recent years, there has been controversy whether multidimensional data such as geometric morphometric data or information on gene expression can be used for estimating phylogenies. This study uses simulations of evolution in multidimensional phenotype spaces to address this question and to identify specific factors that are important for answering it. Most of the simulations use phylogenies with four taxa, so that there are just three possible unrooted trees and the effect of different combinations of branch lengths can be studied systematically. In a comparison of methods, squared-change parsimony performed similarly well as maximum likelihood, and both methods outperformed Wagner and Euclidean parsimony, neighbor-joining and UPGMA. Under an evolutionary model of isotropic Brownian motion, phylogeny can be estimated reliably if dimensionality is high, even with relatively unfavorable combinations of branch lengths. By contrast, if there is phenotypic integration such that most variation is concentrated in one or a few dimensions, the reliability of phylogenetic estimates is severely reduced. Evolutionary models with stabilizing selection also produce highly unreliable estimates, which are little better than picking a phylogenetic tree at random. To examine how these results apply to phylogenies with more than four taxa, we conducted further simulations with up to eight taxa, which indicated that the effects of dimensionality and phenotypic integration extend to more than four taxa, and that convergence among internal nodes may produce additional complications specifically for greater numbers of taxa. Overall, the simulations suggest that multidimensional data, under evolutionary models that are plausible for biological data, do not produce reliable estimates of phylogeny. [Brownian motion; gene expression data; geometric morphometrics; morphological integration; squared-change parsimony; phylogeny; shape; stabilizing selection.].

Phenotypic integration and modularity drives skull shape divergence in the Arctic fox (Vulpes lagopus) from the Commander Islands.

Phenotypic integration and modularity influence morphological disparity and evolvability. However, studies addressing how morphological integration and modularity change for long periods of genetic isolation are scarce. Here, we investigate patterns of phenotypic integration and modularity in the skull of phenotypically and genetically distinct populations of the Artic fox (Vulpes lagopus) from the Commander Islands of the Aleutian belt (i.e. Bering and Mednyi) that were isolated ca 10 000 years by ice-free waters of the Bering sea. We use three-dimensional geometric morphometrics to quantify the strength of modularity and integration from inter-individual variation (static) and from fluctuating asymmetry (random developmental variation) in both island populations compared to the mainland population (i.e. Chukotka) and we investigated how changes in morphological integration and modularity affect disparity and the directionality of trait divergence. Our results indicate a decrease in morphological integration concomitant to an increase in disparity at a developmental level, from mainland to the smallest and farthest population of Mednyi. However, phenotypic integration is higher in both island populations accompanied by a reduction in disparity compared to the population of mainland at a static level. This higher integration may have favoured morphological adaptive changes towards specific feeding behaviours related to the extreme environmental settings of islands. Our study demonstrates how shifts in phenotypic integration and modularity can facilitate phenotypic evolvability at the intraspecific level that may lead to lineage divergence at macroevolutioanry scales.

Mouse Skull Mean Shape and Shape Robustness Rely on Different Genetic Architectures and Different Loci.

The genetic architecture of skull shape has been extensively studied in mice and the results suggest a highly polygenic and additive basis. In contrast few studies have explored the genetic basis of the skull variability. Canalization and developmental stability are the two components of phenotypic robustness. They have been proposed to be emergent properties of the genetic networks underlying the development of the trait itself, but this hypothesis has been rarely tested empirically. Here we use outbred mice to investigate the genetic architecture of canalization of the skull shape by implementing a genome-wide marginal epistatic test on 3D geometric morphometric data. The same data set had been used previously to explore the genetic architecture of the skull mean shape and its developmental stability. Here, we address two questions: (1) Are changes in mean shape and changes in shape variance associated with the same genomic regions? and (2) Do canalization and developmental stability rely on the same loci and genetic architecture and do they involve the same patterns of shape variation? We found that unlike skull mean shape, among-individual shape variance and fluctuating asymmetry (FA) show a total lack of additive effects. They are both associated with complex networks of epistatic interactions involving many genes (protein-coding and regulatory elements). Remarkably, none of the genomic loci affecting mean shape contribute these networks despite their enrichment for genes involved in craniofacial variation and diseases. We also found that the patterns of shape FA and individual variation are largely similar and rely on similar multilocus epistatic genetic networks, suggesting that the processes channeling variation within and among individuals are largely common. However, the loci involved in these two networks are completely different. This in turn underlines the difference in the origin of the variation at these two levels, and points at buffering processes that may be specific to each level.

Epistasis regulates the developmental stability of the mouse craniofacial shape.

Fluctuating asymmetry is a classic concept linked to organismal development. It has traditionally been used as a measure of developmental instability, which is the inability of an organism to buffer environmental fluctuations during development. Developmental stability has a genetic component that influences the final phenotype of the organism and can lead to congenital disorders. According to alternative hypotheses, this genetic component might be either the result of additive genetic effects or a by-product of developmental gene networks. Here we present a genome-wide association study of the genetic architecture of fluctuating asymmetry of the skull shape in mice. Geometric morphometric methods were applied to quantify fluctuating asymmetry: we estimated fluctuating asymmetry as Mahalanobis distances to the mean asymmetry, correcting first for genetic directional asymmetry. We applied the marginal epistasis test to study epistasis among genomic regions. Results showed no evidence of additive effects but several interacting regions significantly associated with fluctuating asymmetry. Among the candidate genes overlapping these interacting regions we found an over-representation of genes involved in craniofacial development. A gene network is likely to be associated with skull developmental stability, and genes originally described as buffering genes (e.g., Hspa2) might occupy central positions within these networks, where regulatory elements may also play an important role. Our results constitute an important step in the exploration of the molecular roots of developmental stability and the first empirical evidence about its genetic architecture.