Assessing Multivariate Constraints to Evolution across Ten Long-Term Avian Studies

Abstract

BackgroundIn a rapidly changing world, it is of fundamental importance to understand processes constraining or facilitating adaptation through microevolution. As different traits of an organism covary, genetic correlations are expected to affect evolutionary trajectories. However, only limited empirical data are available.Methodology/Principal FindingsWe investigate the extent to which multivariate constraints affect the rate of adaptation, focusing on four morphological traits often shown to harbour large amounts of genetic variance and considered to be subject to limited evolutionary constraints. Our data set includes unique long-term data for seven bird species and a total of 10 populations. We estimate population-specific matrices of genetic correlations and multivariate selection coefficients to predict evolutionary responses to selection. Using Bayesian methods that facilitate the propagation of errors in estimates, we compare (1) the rate of adaptation based on predicted response to selection when including genetic correlations with predictions from models where these genetic correlations were set to zero and (2) the multivariate evolvability in the direction of current selection to the average evolvability in random directions of the phenotypic space. We show that genetic correlations on average decrease the predicted rate of adaptation by 28%. Multivariate evolvability in the direction of current selection was systematically lower than average evolvability in random directions of space. These significant reductions in the rate of adaptation and reduced evolvability were due to a general nonalignment of selection and genetic variance, notably orthogonality of directional selection with the size axis along which most (60%) of the genetic variance is found.ConclusionsThese results suggest that genetic correlations can impose significant constraints on the evolution of avian morphology in wild populations. This could have important impacts on evolutionary dynamics and hence population persistence in the face of rapid environmental change.

Rapid adaptive phenotypic change following colonization of a newly restored habitat

“…Body mass has been found to be significantly heritable in the great reed warbler ( Acrocephalus arundinaceus ) as in many other passerine bird species23, and to be a highly evolvable trait23. In our data set, annual mid-parent and offspring body mass is significantly correlated irrespective of annual fluctuations in body mass, which supports the assumption that body mass has a significant heritable component in our population (Supplementary Fig.…”

Patterns of Fluctuating Selection on Morphological and Reproductive Traits in Female Tree Swallow (Tachycineta bicolor)

“…See Table S1 for sample sizes Sequential model building involved testing with likelihood ratio tests (LRTs) (A) the effect of adding twoway interactions between year (coded as factor) and each of all traits and if found significant, then testing (B) the effect of each trait 9 year interaction independently of the other interactions Similar to our findings, the majority of these studies reported selection gradients that were negative for laying date, with earlier laying date being favourable, and positive for clutch size, with larger clutches being beneficial (e.g. different populations in Europe : Sheldon et al 2003;Garant et al 2007;Husby et al 2011b;Teplitsky et al 2011;Porlier et al 2012 Teplitsky et al 2014) being reported for these traits depending on the study system and species studied. Interestingly, the patterns of selection we documented here for morphological traitsselection favours heavier bird, does not affect wing length-are in contrast with the temporal phenotypic trends observed in our study system for females.…”

Reversal of response to artificial selection on body size in a wild passerine

“…1, Table 4). This is in accordance to our expectations, because positive additive genetic covariance between these two traits has earlier been documented in house sparrows (Jensen et al, 2003) (non-significant in males), as well as in quantitative genetics studies of other bird species (Teplitsky et al, 2014). In contrast, neither the two bill traits nor body condition changed in response to correlated selection in the two experimental populations.…”

“…In both populations tarsus length responded as expected in this heritable trait (Jensen et al, 2003Teplitsky et al, 2014). Additionally, wing lengths displayed a small significant correlated response.…”