Rise of dinosaurs reveals major body-size transitions are driven by passive processes of trait evolution

A major macroevolutionary question concerns how long-term patterns of body-size evolution are underpinned by smaller scale processes along lineages. One outstanding long-term transition is the replacement of basal therapsids (stem-group mammals) by archosauromorphs, including dinosaurs, as the dominant large-bodied terrestrial fauna during the Triassic (approx. 252–201 million years ago). This landmark event preceded more than 150 million years of archosauromorph dominance. We analyse a new body-size dataset of more than 400 therapsid and archosauromorph species spanning the Late Permian–Middle Jurassic. Maximum-likelihood analyses indicate that Cope's rule (an active within-lineage trend of body-size increase) is extremely rare, despite conspicuous patterns of body-size turnover, and contrary to proposals that Cope's rule is central to vertebrate evolution. Instead, passive processes predominate in taxonomically and ecomorphologically more inclusive clades, with stasis common in less inclusive clades. Body-size limits are clade-dependent, suggesting intrinsic, biological factors are more important than the external environment. This clade-dependence is exemplified by maximum size of Middle–early Late Triassic archosauromorph predators exceeding that of contemporary herbivores, breaking a widely-accepted ‘rule’ that herbivore maximum size greatly exceeds carnivore maximum size. Archosauromorph and dinosaur dominance occurred via opportunistic replacement of therapsids following extinction, but were facilitated by higher archosauromorph growth rates.

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Within- and among-genus components of size evolution during mass extinction, recovery, and background intervals: a case study of Late Permian through Late Triassic foraminifera

Paleobiology ◽

10.1666/11040.1 ◽

2012 ◽

Vol 38 (4) ◽

pp. 627-643 ◽

Cited By ~ 26

Author(s):

Brianna L. Rego ◽

Steve C. Wang ◽

Demir Altiner ◽

Jonathan L. Payne

Keyword(s):

Mass Extinction ◽

Extinction Risk ◽

Maximum Size ◽

Size Reduction ◽

Late Triassic ◽

Mass Extinctions ◽

Late Permian ◽

Biotic Recovery ◽

Size Evolution ◽

Selective Extinction

One of the best-recognized patterns in the evolution of organismal size is the tendency for mean and maximum size within a clade to decrease following a major extinction event and to increase during the subsequent recovery interval. Because larger organisms are typically thought to be at higher extinction risk than their smaller relatives, it has commonly been assumed that size reduction mostly reflects the selective extinction of larger species. However, to our knowledge the relative importance of within- and among-lineage processes in driving overall trends in body size has never been compared quantitatively. In this study, we use a global, specimen-level database of foraminifera to study size evolution from the Late Permian through Late Triassic. We explicitly decompose size evolution into within- and among-genus components. We find that size reduction following the end-Permian mass extinction was driven more by size reduction within surviving species and genera than by the selective extinction of larger taxa. Similarly, we find that increase in mean size across taxa during Early Triassic biotic recovery was a product primarily of size increase within survivors and the extinction of unusually small taxa, rather than the origination of new, larger taxa. During background intervals we find no strong or consistent tendency for extinction, origination, or within-lineage change to move the overall size distribution toward larger or smaller sizes. Thus, size stasis during background intervals appears to result from small and inconsistent effects of within- and among-lineage processes rather than from large but offsetting effects of within- and among-taxon components. These observations are compatible with existing data for other taxa and extinction events, implying that mass extinctions do not influence size evolution by simply selecting against larger organisms. Instead, they appear to create conditions favorable to smaller organisms.

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Adaptive evolution toward larger size in mammals

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1419823112 ◽

2015 ◽

Vol 112 (16) ◽

pp. 5093-5098 ◽

Cited By ~ 59

Author(s):

Joanna Baker ◽

Andrew Meade ◽

Mark Pagel ◽

Chris Venditti

Keyword(s):

Body Size ◽

Large Body ◽

Biological Species ◽

Directional Bias ◽

Rates Of Evolution ◽

Extant Species ◽

Size Evolution ◽

Mammalian Fossil ◽

Cope’S Rule

The notion that large body size confers some intrinsic advantage to biological species has been debated for centuries. Using a phylogenetic statistical approach that allows the rate of body size evolution to vary across a phylogeny, we find a long-term directional bias toward increasing size in the mammals. This pattern holds separately in 10 of 11 orders for which sufficient data are available and arises from a tendency for accelerated rates of evolution to produce increases, but not decreases, in size. On a branch-by-branch basis, increases in body size have been more than twice as likely as decreases, yielding what amounts to millions and millions of years of rapid and repeated increases in size away from the small ancestral mammal. These results are the first evidence, to our knowledge, from extant species that are compatible with Cope’s rule: the pattern of body size increase through time observed in the mammalian fossil record. We show that this pattern is unlikely to be explained by several nonadaptive mechanisms for increasing size and most likely represents repeated responses to new selective circumstances. By demonstrating that it is possible to uncover ancient evolutionary trends from a combination of a phylogeny and appropriate statistical models, we illustrate how data from extant species can complement paleontological accounts of evolutionary history, opening up new avenues of investigation for both.

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Comparative size evolution of marine clades from the Late Permian through Middle Triassic

Paleobiology ◽

10.1017/pab.2015.36 ◽

2015 ◽

Vol 42 (1) ◽

pp. 127-142 ◽

Cited By ~ 21

Author(s):

Ellen K. Schaal ◽

Matthew E. Clapham ◽

Brianna L. Rego ◽

Steve C. Wang ◽

Jonathan L. Payne

Keyword(s):

Body Size ◽

Middle Triassic ◽

Size Reduction ◽

Late Triassic ◽

Early Triassic ◽

Large Species ◽

Late Permian ◽

Triassic Boundary ◽

Median Size ◽

Permian Extinction

AbstractThe small size of Early Triassic marine organisms has important implications for the ecological and environmental pressures operating during and after the end-Permian mass extinction. However, this “Lilliput Effect” has only been documented quantitatively in a few invertebrate clades. Moreover, the discovery of Early Triassic gastropod specimens larger than any previously known has called the extent and duration of the Early Triassic size reduction into question. Here, we document and compare Permian-Triassic body size trends globally in eight marine clades (gastropods, bivalves, calcitic and phosphatic brachiopods, ammonoids, ostracods, conodonts, and foraminiferans). Our database contains maximum size measurements for 11,224 specimens and 2,743 species spanning the Late Permian through the Middle to Late Triassic. The Permian/Triassic boundary (PTB) shows more size reduction among species than any other interval. For most higher taxa, maximum and median size among species decreased dramatically from the latest Permian (Changhsingian) to the earliest Triassic (Induan), and then increased during Olenekian (late Early Triassic) and Anisian (early Middle Triassic) time. During the Induan, the only higher taxon much larger than its long-term mean size was the ammonoids; they increased significantly in median size across the PTB, a response perhaps related to their comparatively rapid diversity recovery after the end-Permian extinction. The loss of large species in multiple clades across the PTB resulted from both selective extinction of larger species and evolution of surviving lineages toward smaller sizes. The within-lineage component of size decrease suggests that only part of the size decrease can be related to the end-Permian kill mechanism; in addition, Early Triassic environmental conditions or ecological pressures must have continued to favor small body size as well. After the end-Permian extinction, size decrease occurred across ecologically and physiologically disparate clades, but this size reduction was limited to the first part of the Early Triassic (Induan). Nektonic habitat or physiological buffering capacity may explain the contrast of Early Triassic size increase and diversification in ammonoids versus size reduction and slow recovery in benthic clades.

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The Evolution of Primate Body Size: Left-skewness, Maximum Size, and Cope’s Rule

10.1101/092866 ◽

2016 ◽

Author(s):

Richard C. Tillquist ◽

Lauren G. Shoemaker ◽

Kevin Bracy Knight ◽

Aaron Clauset

Keyword(s):

Body Size ◽

Size Distribution ◽

Maximum Size ◽

The Body ◽

Skewed Distribution ◽

Primate Species ◽

Opposite Pattern ◽

Evolutionary Characteristic ◽

Initial Tendency ◽

Cope’S Rule

Body size is a key physiological, ecological, and evolutionary characteristic of species. Within most major clades, body size distributions follow a right-skewed pattern where most species are relatively small while a few are orders of magnitude larger than the median size. Using a novel database of 742 extant and extinct primate species’ sizes over the past 66 million years, we find that primates exhibit the opposite pattern: a left-skewed distribution. We investigate the long-term evolution of this distribution, first showing that the initial size radiation is consistent with plesiadapiformes (an extinct group with an uncertain ancestral relationship to primates) being ancestral to modern primates. We calculate the strength of Cope’s Rule, showing an initial tendency for descendants to increase in size relative to ancestors until the trend reverses 40 million years ago. We explore when the primate size distribution becomes left-skewed and study correlations between body size patterns and climactic trends, showing that across Old and New World radiations the body size distribution initially exhibits a right-skewed pattern. Left-skewness emerged early in Old World primates in a manner consistent with a previously unidentified possible maximum body size, which may be mechanistically related to primates’ encephalization and complex social groups.

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Effects of allometry, productivity and lifestyle on rates and limits of body size evolution

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2013.1007 ◽

2013 ◽

Vol 280 (1764) ◽

pp. 20131007 ◽

Cited By ~ 20

Author(s):

Jordan G. Okie ◽

Alison G. Boyer ◽

James H. Brown ◽

Daniel P. Costa ◽

S. K. Morgan Ernest ◽

...

Keyword(s):

Body Size ◽

Generation Time ◽

Allometric Scaling ◽

Empirical Work ◽

Morphological Diversity ◽

Maximum Size ◽

Scaling Exponent ◽

Size Evolution ◽

Body Size Evolution ◽

Maximum Body

Body size affects nearly all aspects of organismal biology, so it is important to understand the constraints and dynamics of body size evolution. Despite empirical work on the macroevolution and macroecology of minimum and maximum size, there is little general quantitative theory on rates and limits of body size evolution. We present a general theory that integrates individual productivity, the lifestyle component of the slow–fast life-history continuum, and the allometric scaling of generation time to predict a clade's evolutionary rate and asymptotic maximum body size, and the shape of macroevolutionary trajectories during diversifying phases of size evolution. We evaluate this theory using data on the evolution of clade maximum body sizes in mammals during the Cenozoic. As predicted, clade evolutionary rates and asymptotic maximum sizes are larger in more productive clades (e.g. baleen whales), which represent the fast end of the slow–fast lifestyle continuum, and smaller in less productive clades (e.g. primates). The allometric scaling exponent for generation time fundamentally alters the shape of evolutionary trajectories, so allometric effects should be accounted for in models of phenotypic evolution and interpretations of macroevolutionary body size patterns. This work highlights the intimate interplay between the macroecological and macroevolutionary dynamics underlying the generation and maintenance of morphological diversity.

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Body-size evolution in Cretaceous molluscs and the status of Cope's rule

Nature ◽

10.1038/385250a0 ◽

1997 ◽

Vol 385 (6613) ◽

pp. 250-252 ◽

Cited By ~ 171

Author(s):

David Jablonski

Keyword(s):

Body Size ◽

Size Evolution ◽

The Status ◽

Body Size Evolution ◽

Cope’S Rule

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Golden Orbweavers Ignore Biological Rules: Phylogenomic and Comparative Analyses Unravel a Complex Evolution of Sexual Size Dimorphism

10.1101/368233 ◽

2018 ◽

Cited By ~ 3

Author(s):

Matjaž Kuntner ◽

Chris A. Hamilton ◽

Cheng Ren-Chung ◽

Matjaž Gregorič ◽

Nik Lupše ◽

...

Keyword(s):

Body Size ◽

Female Body ◽

Sexual Size Dimorphism ◽

Female Size ◽

Male And Female ◽

Size Dimorphism ◽

Female Body Size ◽

Size Evolution ◽

Web Size ◽

Cope’S Rule

AbstractInstances of sexual size dimorphism (SSD) provide the context for rigorous tests of biological rules of size evolution, such as Cope’s Rule (phyletic size increase), Rensch’s Rule (allometric patterns of male and female size), as well as male and female body size optima. In certain spider groups, such as the golden orbweavers (Nephilidae), extreme female-biased SSD (eSSD, female:male body length ≥ 2) is the norm. Nephilid genera construct webs of exaggerated proportions which can be aerial, arboricolous, or intermediate (hybrid). First, we established the backbone phylogeny of Nephilidae using 367 Anchored Hybrid Enrichment (AHE) markers, then combined these data with classical markers for a reference species-level phylogeny. Second, we used the phylogeny to test Cope and Rensch’s Rules, sex specific size optima, and the coevolution of web size, type, and features with female and male body size and their ratio, SSD. Male, but not female, size increases significantly over time, and refutes Cope’s Rule. Allometric analyses reject the converse, Rensch’s Rule. Male and female body sizes are uncorrelated. Female size evolution is random, but males evolve towards an optimum size (3.2–4.9 mm). Overall, female body size correlates positively with absolute web size. However, intermediate sized females build the largest webs (of the hybrid type), giant female Nephila and Trichonephila build smaller webs (of the aerial type), and the smallest females build the smallest webs (of the arboricolous type). We propose taxonomic changes based on the criteria of clade age, monophyly and exclusivity, classification information content, diagnosability, and arachnological community practice. We resurrect the family Nephilidae Simon 1894 that contains Clitaetra Simon 1889, the Cretaceous Geratonephila Poinar & Buckley 2012, Herennia Thorell 1877, Indoetra Kuntner 2006, new rank, Nephila Leach 1815, Nephilengys L. Koch 1872, Nephilingis Kuntner 2013, and Trichonephila Dahl 1911, new rank. We propose the new clade Orbipurae to contain Araneidae Clerck 1757, Phonognathidae Simon 1894, new rank, and Nephilidae. Nephilid female gigantism is a phylogenetically-ancient phenotype (over 100 ma), as is eSSD, though their magnitudes vary by lineage and, to some extent, biogeographically.

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Environmental and scale-dependent evolutionary trends in the body size of crustaceans

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2015.0440 ◽

2015 ◽

Vol 282 (1811) ◽

pp. 20150440 ◽

Cited By ~ 15

Author(s):

Adiël A. Klompmaker ◽

Carrie E. Schweitzer ◽

Rodney M. Feldmann ◽

Michał Kowalewski

Keyword(s):

Body Size ◽

Ecological Impact ◽

The Body ◽

Minimum Size ◽

Brachyuran Crab ◽

Species Sorting ◽

Size Evolution ◽

Body Sizes

The ecological and physiological significance of body size is well recognized. However, key macroevolutionary questions regarding the dependency of body size trends on the taxonomic scale of analysis and the role of environment in controlling long-term evolution of body size are largely unknown. Here, we evaluate these issues for decapod crustaceans, a group that diversified in the Mesozoic. A compilation of body size data for 792 brachyuran crab and lobster species reveals that their maximum, mean and median body size increased, but no increase in minimum size was observed. This increase is not expressed within lineages, but is rather a product of the appearance and/or diversification of new clades of larger, primarily burrowing to shelter-seeking decapods. This argues against directional selective pressures within lineages. Rather, the trend is a macroevolutionary consequence of species sorting: preferential origination of new decapod clades with intrinsically larger body sizes. Furthermore, body size evolution appears to have been habitat-controlled. In the Cretaceous, reef-associated crabs became markedly smaller than those in other habitats, a pattern that persists today. The long-term increase in body size of crabs and lobsters, coupled with their increased diversity and abundance, suggests that their ecological impact may have increased over evolutionary time.

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