Evolutionary mode routinely varies among morphological traits within fossil species lineages

Abstract

Recent studies have revitalized interest in methods for detecting evolutionary modes in both fossil sequences and phylogenies. Most of these studies examine single size or shape traits, often implicitly assuming that single phenotypic traits are adequate representations of species-level change. We test the validity of this assumption by tallying the frequency with which traits vary in evolutionary mode within fossil species lineages. After fitting models of directional change, unbiased random walk, and stasis to a dataset of 635 traits across 153 species lineages, we find that within the majority of lineages, evolutionary mode varies across traits and the likelihood of conflicting within-lineage patterns increases with the number of traits analyzed. In addition, single traits may show variation in evolutionary mode even in situations where the overall morphological evolution of the lineage is dominated by one type of mode. These quantified, stratigraphically based findings validate the idea that morphological patterns of mosaic evolution are pervasive across groups of organisms throughout Earth's history.integration | modularity | punctuated equilibrium | rate of evolution | trends M uch of the research on stasis and punctuated equilibrium has focused on processes that could generate or influence patterns of morphological evolution, including stabilizing selection (1, 2), metapopulation dynamics (3), environmental stability, habitat tracking, and stress (3-6). Recently, however, renewed discussions have highlighted the patterns themselves. These investigations largely fall into one of two categories, each focusing on a different aspect of the theory of punctuated equilibrium (7,8). The first considers whether morphological evolution is concentrated at speciation events or occurs gradually along branches of a phylogenetic tree. Here, methods applied to trees of extant taxa test whether the variance in phenotypes increases as a function of the number of speciation events (inferring a punctuational mode) or of total branch length, i.e., time (inferring a gradualist mode) (9-13). The second category distinguishes morphological evolutionary patterns within sequences of populations in the fossil record, particularly to determine the relative frequency of stasis compared with other modes of change. Recent methods either expand on earlier work in treating unbiased random walks as null hypotheses [e.g., Hurst measure (14), see ref. 15 for earlier work] or treat an unbiased random walk as a model of evolutionary change to be judged alongside other models using model selection criteria (16)(17)(18).What studies in both categories have in common is that the quantitative assessment of morphological change is mostly based on single traits, either size or shape. In our dataset of 635 sequences compiled from literature on the fossil record, only 17% were derived using multivariate analysis of several traits (Dataset S1). The remaining sequences are comprised primarily of trait lengths and trait length:length ratios (Dataset S1)...

Morphological stasis in an ongoing gastropod radiation from Lake Malawi

“…Regardless of the actual timing of divergence between these species, our results indicate that different traits have evolved differently during this young radiation (see also ref. 13).…”

New Cricetodontini from the middle Miocene of Europe: an example of mosaic evolution

“…This consists in different rates of change in the jugal teeth, which result in a degree of uncoupling between the upper and lower features (Stebbins 1983, López Martínez 1997, Hopkins & Lidgard 2012. Furthermore, this mosaic evolution is also recognized in other Cricetodontini from the European late Aragonian (De Bruijn et al 1993, De Bruijn & Ünay 1996.…”

Simple versus complex models of trait evolution and stasis as a response to environmental change

“…Method development focused on three canonical models germane to punctuated equilibrium: stasis, directional or sustained gradual change, and an intermediate model of a random walk. Two recent compilations found much more support for stasis than gradual evolution on paleontological timescales; in only 5% of cases was directional evolution the best supported model, with the remaining sequences divided almost equally between random walks and stasis (14,15).These compilations helped to resolve some lingering issues, but they have an important limitation in that they applied a rather restricted set of models. Stasis, random walks, and directional change are simple models in the sense that they require few parameters to specify, and also in that they each imply uniform evolutionary dynamics within fossil sequences (16).…”

“…Method development focused on three canonical models germane to punctuated equilibrium: stasis, directional or sustained gradual change, and an intermediate model of a random walk. Two recent compilations found much more support for stasis than gradual evolution on paleontological timescales; in only 5% of cases was directional evolution the best supported model, with the remaining sequences divided almost equally between random walks and stasis (14,15).…”