Evolutionary Persistence of Phenotypic Integration: Influence of Developmental and Functional Relationships on Complex Trait Evolution

Abstract

Abstract. Examination of historical persistence of integration patterns provides an important insight into understanding the origin and evolution of complex traits. Specifically, the distinct effects of developmental and functional integration on the evolution of complex traits are often overlooked. Because patterns of functional integration are commonly shaped by selection exerted by the external environment, whereas patterns of developmental integration can be determined by relatively environment-independent selection for developmental homeostasis, examination of historical persistence of morphological integration patterns among species should reveal the relative importance of current selection in the evolution of complex traits. We compared historical persistence of integration patterns produced by current developmental versus ecological requirements by examining the evolution of complex mandibular structures in nine species of soricid shrews. We found that, irrespective of phylogenetic relatedness of species, patterns of developmental and functional integration were highly concordant, suggesting that strong selection for developmental homeostasis favors concordant channeling of both internal and external variation. Overall, our results suggest that divergence in mandible shape among species closely follows variation in functional demands and ecological requirements regardless of phylogenetic relatedness among species.

Analyzing Fluctuating Asymmetry with Geometric Morphometrics: Concepts, Methods, and Applications

“…Analyses of covariation in the asymmetries of landmark configurations thus can be used to infer whether such developmental interactions exist (Section 6). This approach has been applied in a growing number of studies [11,16,44,49,51,56,59,63,67,72,74,75,78,79,82,139,[167][168][169][170][171][172][173][174].…”

“…Many studies have found matrix correlations between covariance matrices for fluctuating asymmetry and individual variation that are statistically significant, but of rather variable strengths [11,16,44,49,55,56,67,72,79,82,97,106,119,139,[167][168][169]172,173,177,358]. A few studies have reported a mix of significant and non-significant results for analyses of multiple samples or structures [54,75,120,174], and some other studies found only non-significant test results [13,42,73,78].…”

“…After some pioneering studies of integration in fluctuating asymmetry [400,401], interest in the topic grew quickly since the late 1990s, mostly in the context of evolutionary developmental biology, where analyses of covariation of fluctuating asymmetry, particularly in combination with the methods of geometric morphometrics, are now a standard tool in the study of morphological integration [11,16,17,42,44,49,51,55,135,168,169,176,251,402,403]. The rationale behind using fluctuating asymmetry in studies of morphological integration is that it can provide information on the developmental origins of covariation among traits [17,404].…”

Studying morphological integration and modularity at multiple levels: concepts and analysis

“…Because fluctuating asymmetry originates from random variation in developmental processes, the asymmetries of different traits are correlated only if there are direct interactions between developmental pathways that produce the traits [46,47]. This approach has been applied in a broad range of animal systems [10,[12][13][14][15]27,36,37,[48][49][50][51][52][53][54][55]. Whereas this reasoning applies widely to motile organisms, including most animals, caution is necessary in applying it to sessile organisms like most plants, where a part of fluctuating asymmetry may be due to plastic responses to heterogeneity in microenvironmental factors [25,56].…”

Multivariate segregation analysis for quantitative traits in line crosses

“…Certain combinations of traits rarely occur randomly: they may be selected for their coordinated function or have a common genetic basis such as pleiotropy (Mclellan, 2005). Trait integration produced by a shared genetic basis is usually independent of the environment, whereas integration caused by functional association may vary across environments (Young and Badyaev, 2006). However, it cannot be concluded that traits evolve independently if only residual correlation is detected in a single experiment.…”