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Developmental bias, macroevolution, and the fossil record

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Abstract

A fuller understanding of the role of developmental bias in shaping large‐scale evolutionary patterns requires integrating bias (the probability distribution of variation accessible to an ancestral phenotype) with clade dynamics (the differential survival and production of species and evolutionary lineages). This synthesis could proceed as a two‐way exchange between the developmental data available to neontologists and the strictly phenotypic but richly historical and dynamic data available to paleontologists. Analyses starting in extant populations could aim to predict macroevolution in the fossil record from observed developmental bias, while analyses starting in the fossil record, particularly the record of extant species and lineages, could aim to predict developmental bias from macroevolutionary patterns, including the broad range of extinct phenotypes. Analyses in multivariate morphospaces are especially effective when coupled with phylogeny, theoretical and developmental models, and diversity–disparity plots. This research program will also require assessing the “heritability” of an ancestral bias across phylogeny, and the tendency for bias change in strength and orientation over evolutionary time. Such analyses will help find a set of general rules for the macroevolutionary effects of developmental bias, including its impact on and interactions with the other intrinsic and extrinsic factors governing the movement, expansion, and contraction of clades in morphospace. HIGHLIGHTS • A fuller, more synthetic understanding of the macroevolutionary role of developmental bias requires the integration of bias with clade dynamics—that is, the differential survival and production of species and evolutionary lineages

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... Some groups, once evolved, seem constrained in morphospace, whereas previously occupied regions of morphospaces, once vacated, are sometimes not reoccupied. Although these patterns are the combined outcome of both evolvability and ecological success or failure (i.e., selection), the relevance of evolvability explanations has long been recognized, usually considered in terms of constraints-the lack of evolvability in some guise (Raup 1967;Blake 1980;Maynard Smith et al. 1985;Gould 1989;Allmon and Ross 1990;Erwin 2007;Vermeij 2015;Wright 2017;Jablonski 2020;see Brigandt [2015] about the usage shift from constraint to evolvability and on the relationship between these two concepts). The connection between morphospace exploration and evolvability has been perhaps most explicit in discussions of the dramatic explosion of disparity in the Cambrian Period. ...
... Proximate developmental processes that underpin major evolutionary transitions have been inferred for an increasing number of examples, such as the mammalian inner ear (Luo 2011;Luo et al. 2015;Urban et al. 2017;Wang et al. 2019Wang et al. , 2021Le Maitre et al. 2020), arthropod segmentation (Chipman and Edgecombe 2019), tetrapod limbs (Stewart et al. 2020), and turtle shells (Lyson and Bever 2020; Schoch and Sues 2020). Insights from these paleo-evo-devo studies provide a richer understanding of how evolutionary novelties arise and their importance in the history of life (Erwin 2012;Urdy et al. 2013;Wagner 2014;Jablonski 2020). However, cases in which researchers use developmental information to make predictions about the generation of phenotypic variation are most relevant to the topic of evolvability. ...
... Taxonomic differences have been documented for genetic features related to evolvability, such as overall rates of mutation (Lynch 2010) and recombination (Stapley et al. 2017). Developmental or morphological features that have been associated with evolvability differences among clades include growth strategy in regular versus irregular echinoids (Hopkins and Smith 2015), the loosening of allometric relationships (Tsuboi et al. 2018), and the breaking of left-right symmetry in bivalves (Jablonski 2020). ...
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The concept of evolvability—the capacity of a population to produce and maintain evolutionarily relevant variation—has become increasingly prominent in evolutionary biology. Paleontology has a long history of investigating questions of evolvability, but paleontological thinking has tended to neglect recent discussions, because many tools used in the current evolvability literature are challenging to apply to the fossil record. The fundamental difficulty is how to disentangle whether the causes of evolutionary patterns arise from variational properties of traits or lineages rather than being due to selection and ecological success. Despite these obstacles, the fossil record offers unique and growing sources of data that capture evolutionary patterns of sustained duration and significance otherwise inaccessible to evolutionary biologists. Additionally, there exist a variety of strategic possibilities for combining prominent neontological approaches to evolvability with those from paleontology. We illustrate three of these possibilities with quantitative genetics, evolutionary developmental biology, and phylogenetic models of macroevolution. In conclusion, we provide a methodological schema that focuses on the conceptualization, measurement, and testing of hypotheses to motivate and provide guidance for future empirical and theoretical studies of evolvability in the fossil record.
... Much of evolutionary theory has focused on this second step. By contrast, the study of variation has been relatively underdeveloped (Smith et al. 1985;Wagner and Altenberg 1996;Gould 2002;Laland et al. 2014;McCandlish and Stoltzfus 2014;Wagner 2014;Love 2015;Charlesworth et al. 2017;Stoltzfus 2019;Uller et al. 2018;Svensson and Berger 2019;Uller and Laland 2019;Jablonski 2020). If the variation is unstructured, or isotropic, then this lacuna would be unproblematic. ...
... On the other hand, if there are strong anisotropic developmental biases, then structure in the arrival of variation may well play an important explanatory role in the biological phenomena we observe today. Although the discussion of how anisotropic variation affects adaptive evolutionary outcomes has moved on significantly from the days of Gould's critique, primarily due to the growth of the field of evo-devo (Love 2015), it remains a source of significant contention (Laland et al. 2014;McCandlish and Stoltzfus 2014;Love 2015;Charlesworth et al. 2017;Stoltzfus 2019;Uller et al. 2018;Svensson and Berger 2019;Uller and Laland 2019;Jablonski 2020). ...
... The fundamental reason for the anisotropic occupation of a morphospace could simply be some form of contingency, where the evolution started at one point in the morphospace and did not have enough time to fully explore the space. Or it could be some more predictable cause, such as natural selection disfavoring certain characteristics, or else developmental bias favoring certain types of variation (Uller et al. 2018;Jablonski 2020). ...
Article
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Morphospaces –representations of phenotypic characteristics– are often populated unevenly, leaving large parts unoccupied. Such patterns are typically ascribed to contingency, or else to natural selection disfavouring certain parts of the morphospace. The extent to which developmental bias, the tendency of certain phenotypes to preferentially appear as potential variation, also explains these patterns is hotly debated. Here we demonstrate quantitatively that developmental bias is the primary explanation for the occupation of the morphospace of RNA secondary structure (SS) shapes. Upon random mutations, some RNA SS shapes (the frequent ones) are much more likely to appear than others. By using the RNAshapes method to define coarse-grained SS classes, we can directly compare the frequencies that non-coding RNA SS shapes appear in the RNAcentral database to frequencies obtained upon random sampling of sequences. We show that: a) Only the most frequent structures appear in nature; the vast majority of possible structures in the morphospace have not yet been explored. b) Remarkably small numbers of random sequences are needed to produce all the RNA SS shapes found in nature so far. c) Perhaps most surprisingly, the natural frequencies are accurately predicted, over several orders of magnitude in variation, by the likelihood that structures appear upon uniform random sampling of sequences. The ultimate cause of these patterns is not natural selection, but rather strong phenotype bias in the RNA genotype-phenotype map, a type of developmental bias or “findability constraint”, which limits evolutionary dynamics to a hugely reduced subset of structures that are easy to “find”.
... Some groups, once evolved, seem constrained in morphospace, whereas previously occupied regions of morphospaces, once vacated, are sometimes not reoccupied. Although these patterns are the combined outcome of both evolvability and ecological success or failure (i.e., selection), the relevance of evolvability explanations has long been recognized, usually considered in terms of constraints-the lack of evolvability in some guise (Raup 1967;Blake 1980;Maynard Smith et al. 1985;Gould 1989;Allmon and Ross 1990;Erwin 2007;Vermeij 2015;Wright 2017;Jablonski 2020;see Brigandt [2015] about the usage shift from constraint to evolvability and on the relationship between these two concepts). The connection between morphospace exploration and evolvability has been perhaps most explicit in discussions of the dramatic explosion of disparity in the Cambrian Period. ...
... Proximate developmental processes that underpin major evolutionary transitions have been inferred for an increasing number of examples, such as the mammalian inner ear (Luo 2011;Luo et al. 2015;Urban et al. 2017;Wang et al. 2019Wang et al. , 2021Le Maitre et al. 2020), arthropod segmentation (Chipman and Edgecombe 2019), tetrapod limbs (Stewart et al. 2020), and turtle shells (Lyson and Bever 2020; Schoch and Sues 2020). Insights from these paleo-evo-devo studies provide a richer understanding of how evolutionary novelties arise and their importance in the history of life (Erwin 2012;Urdy et al. 2013;Wagner 2014;Jablonski 2020). However, cases in which researchers use developmental information to make predictions about the generation of phenotypic variation are most relevant to the topic of evolvability. ...
... Taxonomic differences have been documented for genetic features related to evolvability, such as overall rates of mutation (Lynch 2010) and recombination (Stapley et al. 2017). Developmental or morphological features that have been associated with evolvability differences among clades include growth strategy in regular versus irregular echinoids (Hopkins and Smith 2015), the loosening of allometric relationships (Tsuboi et al. 2018), and the breaking of left-right symmetry in bivalves (Jablonski 2020). ...
... Macroevolutionary studies aim to explain the drivers of largescale biological phenomena and often rely on fossils to elucidate the complex processes determining modern biodiversity. [1][2][3] One frequently documented pattern is for closely related clades to manifest different radiation profiles over their extended geologic history. [4][5][6] A notable example is the extreme asymmetry in species richness evident between modern lamniform and carcharhiniform sharks. ...
... 46 2. A dignathic model (n Lamniformes = 1196) differentiating the upper and lower dental units. 3. A combined-heterodonty model (n Lamniformes = 907) allowing for interaction between tooth positions and dental units. ...
... Even though these constraints were originally thought to be overcome with time (Felsenstein 1988;Schluter 1996;Arnold et al. 2001), we have recently seen a plethora of results suggesting that genetic and ontogenetic constraints might affect large-scale macroevolutionary patterns (Marroig and Cheverud 2004;Firmat et al. 2014;Simon et al. 2016;De Azevedo et al. 2017;Houle et al. 2017;McGlothlin et al. 2018). This has instigated a resurgence of interest in the effect of intrinsic constraints on macroevolution Jablonski 2019). Therefore, how constraints might have affected morphological adaptation is an issue that requires further attention. ...
... The role of the association among parts in shaping macroevolutionary patterns has always been a topic of intense debate (Gould and Lewontin 1979;Maynard Smith et al. 1985;Jablonski 2019). While covariances between Note: Linear model shows results of the nonparametric RRPP multiple regression of the relationship between morphology and diet. ...
Article
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The association between phenotype and ecology is essential for understanding the environmental drivers of morphological evolution. This is a particularly challenging task when dealing with complex traits, such as the skull, where multiple selective pressures are at play and evolution might be constrained by ontogenetic and genetic factors. I integrate morphometric tools, comparative methods, and quantitative genetics to investigate how ontogenetic constraints and selection might have interacted during the evolution of the skull in extant Canidae. The results confirm that the evolution of cranial morphology was largely adaptive and molded by changes in diet composition. While the investigation of the adaptive landscape reveals two main selective lines of least resistance (one associated with size and one associated with functional shape features), rates of evolution along size were higher than those found for shape dimensions, suggesting the influence of constraints on morphological evolution. Structural modeling analyses revealed that size, which is the line of most genetic/phenotypic variation, might have acted as a constraint, negatively impacting dietary evolution. Constraints might have been overcome in the case of selection for the consumption of large prey by associating strong selection along both size and shape directions. The results obtained here show that microevolutionary constraints may have played a role in shaping macroevolutionary patterns of morphological evolution.
... Macroevolutionary studies aim to explain the drivers of largescale biological phenomena and often rely on fossils to elucidate the complex processes determining modern biodiversity. [1][2][3] One frequently documented pattern is for closely related clades to manifest different radiation profiles over their extended geologic history. [4][5][6] A notable example is the extreme asymmetry in species richness evident between modern lamniform and carcharhiniform sharks. ...
... 46 2. A dignathic model (n Lamniformes = 1196) differentiating the upper and lower dental units. 3. A combined-heterodonty model (n Lamniformes = 907) allowing for interaction between tooth positions and dental units. ...
Article
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Sharks are iconic predators in today’s oceans, yet their modern diversity has ancient origins. In particular, present hypotheses suggest that a combination of mass extinction, global climate change, and competition has regulated the community structure of dominant mackerel (Lamniformes) and ground (Carcharhiniformes) sharks over the last 66 million years. However, while these scenarios advocate an interplay of major abiotic and biotic events, the precise drivers remain obscure. Here, we focus on the role of feeding ecology using a geometric morphometric analysis of 3,837 fossil and extant shark teeth. Our results reveal that morphological segregation rather than competition has characterized lamniform and carcharhiniform evolution. Moreover, although lamniforms suffered a long-term disparity decline potentially linked to dietary “specialization,” their recent disparity rivals that of “generalist” carcharhiniforms. We further confirm that low eustatic sea levels impacted lamniform disparity across the end-Cretaceous mass extinction. Adaptations to changing prey availability and the proliferation of coral reef habitats during the Paleogene also likely facilitated carcharhiniform dispersals and cladogenesis, underpinning their current taxonomic dominance. Ultimately, we posit that trophic partitioning and resource utilization shaped past shark ecology and represent critical determinants for their future species survivorship.
... The predictability of morphological variation across evolution builds upon the classic notion of Morphological Integration that Olson and Miller (1958) proposed to mathematically underscore evolutionary constraints from the fossil record. Today, there is little doubt that the evolution of morphology reflects the evolution of developmental pathways (Waddington 1975;Erwin 2007;Young 2017;Jablonski 2020), which, in turn, entails that the biased occupation of available morphospace is the product of restricted epigenetic pathways (Hallgrímsson et al. 2009). The 'Raupian' question would be if these findings require an adaptive explanation or any causal explanation at all (Erwin 2015). ...
Article
Synapsida represents a rich lineage of tetrapods including a mixture of morphotypes, from reptilian-like ‘pelycosaurs’ to crown group mammals, spanning more than 325 My. Although such a morphological diversity peaked several times across three eras, little is known about the constraints underlying such evolutionary patterns. Using theoretical morphology rationales, we assessed the distribution of skull disparity by measuring three functional partitions (i.e. rostrum, orbit and braincase) in a sample encompassing most major clades of the lineage (n = 169). To broaden our macroevolutionary scope, we compared this pattern with that of the archosaurian sauropsids (Diapsida). Results show that despite being less diverse, the disparity of synapsid skulls almost doubles that of the archosaurs. The synapsids span an outstanding range of facial proportions, involving short faces (newly labelled parvirostral) and extreme shortening of the face in some primates, including humans, contributing less than 10% to skull geometry (microrostral). We also found that synapsids changed their geometric rules of skull organisation; in the Permo-Trias, the orbit and the braincase changed concomitantly, as in the diapsids, hence being more ‘reptilian’. Thereafter, depleting the orbit from craniofacial variation at the transition to therian mammals, in the Mesozoic, marked an evolutionary pathway that endured throughout the Cenozoic.
... La correlazione deriva dalla necessità di mantenere costante l'interazione tra le due proteine, ciò fa sì che una modifica di A deve essere accoppiata a una modifica di B perché il sistema AB rimanga funzionale (Goh et al., 2000). In biologia le modifiche macroscopiche (ciò che si definisce "macro-evoluzione", per distinguerla dalla "micro-evoluzione" che lascia sostanzialmente intatta la forma generale del sistema) sono infinitamente più rare e, non a caso, la dinamica del loro insorgere è ancora fortemente dibattuta (Hautmann, 2020;Jablonski, 2020). Richiamando il concetto di "regole dell'arte", possiamo paragonare le micro-evoluzioni alla complessità delle procedure di autorizzazione necessarie per una piccola modifica di un'abitazione pre-esistente; le macro-evoluzioni corrispondono invece alle complesse procedure di autorizzazione necessarie per sconvolgere un intero quartiere costruendo una piazza o un grattacielo (Giuliani & Modonesi, 2011). ...
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Con saggi di Alessandro Giuliani, Pier Christian Verde e...Vladimir Nabokov Da un punto di vista clinico il lavoro dello psicologo può essere descritto in termini di osservazione del materiale psichico del paziente, ascolto dello stesso attraverso il filtro della mente del clinico, e sua restituzione in seduta. “Osservazione, Ascolto ed Interpretazione” indaga il tema di come si possa divenire buoni lettori del materiale clinico di un paziente individuale o di un gruppo mostrando il posizionamento scientifico necessario a favorire lo sviluppo della relazione terapeutica. Come si osserva il materiale psichico? Qual è l’attitudine necessaria a favorire la scoperta di qualcosa di nuovo? Come lo si interpreta? Il volume risponde a tali annose questioni attraverso un confronto interdisciplinare. Il testo, unico nel suo genere, mostra infatti come si possa divenire buoni lettori di un materiale clinico, di un insieme di dati empirico, di un testo di letteratura. Non dovremmo mai dimenticare infatti che l’“opera d’arte”, indipendentemente dal dominio scientifico a cui appartiene, è sempre la creazione di un mondo nuovo, e non lo si dovrebbe confondere con le cose che si sanno già. L’artista entusiasta tende ad avere un atteggiamento troppo soggettivo, mentre una freddezza di giudizio scientifica attenuerà il calore dell’intuizione. Per trarre piacere da quell’opera d’arte l’aspirante buon lettore dovrà perciò munirsi di passione e pazienza, la passione dell’artista e la pazienza dello scienziato. Buona lettura. [With contributions by Alessandro Giuliani, Pier Christian Verde and...Vladimir Nabokov From a clinical point of view, the work of a psychologist can be described in terms of observation of the patient's psychic material, listening to it through the filter of the clinician's mind, and commenting or interpreting it back to the patient. “Observation, Listening and Interpretation” investigates how we can become good readers of the clinical material of an individual patient or a group, by showing the scientific stance needed to promote the development of the therapeutic relationship. How should we observe the clinical material? What is the attitude needed to encourage the discovery of something new? How should we comment the clinical material? The volume responds to these long-standing questions through an interdisciplinary discussion. The book, one of a kind, in fact shows how we can become good readers of a clinical material; of a set of empirical data; of a literary text. We should never forget that a "masterpiece", regardless of the scientific domain to which it belongs, is always the creation of a new world, and should not be confused with things that are already known. The enthusiastic artist tends to have a too subjective attitude, while the coldness of scientific judgment will attenuate the warmth of intuition. To feel pleasure from that masterpiece, the aspiring good reader will therefore have to equip himself with passion and patience; the passion of the artist and the patience of the scientist. Enjoy the reading.]
... Finally, this chapter also attempts to do historical justice to all those assumptions stated under the name of "orthogenesis," considering that it has been demonstrated by this and other works that orthogenesis was not a "metaphysical," "vitalistic," or "theological" theory with "progressive" connotations (Grehan and Ainsworth 1985;Gould 2002;Levit and Olsson 2006;Popov 2009Popov , 2018De Renzi 2014;Ochoa and Barahona 2014;Ulett 2014Ulett , 2016Ochoa 2017;Ceccarelli 2021). Rather, it was a theory that describes the evolutionary trends that exist in the evolution of lineages which today we recognize phenomenologically under the term of "parallelism" (Wake et al. 2011;Ochoa and Rasskin-Gutman 2015;Monnet et al. 2015), and whose causes are probably due to the developmental bias (Arthur 2004;Jablonski 2020; Moczek 2020), sometimes along with a little help from natural selection. ...
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George Gaylord Simpson, one of the architects of Modern Synthesis, was one of the main figures of paleontology who discredited and rejected the theory of orthogenesis in his discipline. Following the neo-Darwinian agenda, he thought that this theory had little basis to be proven. Since then, orthogenesis has been defined in textbooks as a “metaphysical,” “vitalistic,” or “theological” theory. However, in the present analysis, I demonstrate that Simpson indirectly advocated for an explanation of orthogenesis through his explanation of the concept of “parallelism.” In other words, Simpson did not end orthogenesis but rather ended up defending the phenomenon of orthogenesis through the concept of parallelism. I argue that Simpson maintained pluralistic ideas upon including constraints into his evolutionary system as a complementary factor to the argument of natural selection.
... Very few such fundamental growth patterns exist, including logarithmic spiral growth [6,7]. These growth patterns are important because they significantly influence the diversity of life by making some phenotypes very common while constraining or even prohibiting others, essentially favouring specific evolutionary trajectories [1,[8][9][10][11][12][13]. ...
Article
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Background A major goal of evolutionary developmental biology is to discover general models and mechanisms that create the phenotypes of organisms. However, universal models of such fundamental growth and form are rare, presumably due to the limited number of physical laws and biological processes that influence growth. One such model is the logarithmic spiral, which has been purported to explain the growth of biological structures such as teeth, claws, horns, and beaks. However, the logarithmic spiral only describes the path of the structure through space, and cannot generate these shapes. Results Here we show a new universal model based on a power law between the radius of the structure and its length, which generates a shape called a ‘power cone’. We describe the underlying ‘power cascade’ model that explains the extreme diversity of tooth shapes in vertebrates, including humans, mammoths, sabre-toothed cats, tyrannosaurs and giant megalodon sharks. This model can be used to predict the age of mammals with ever-growing teeth, including elephants and rodents. We view this as the third general model of tooth development, along with the patterning cascade model for cusp number and spacing, and the inhibitory cascade model that predicts relative tooth size. Beyond the dentition, this new model also describes the growth of claws, horns, antlers and beaks of vertebrates, as well as the fangs and shells of invertebrates, and thorns and prickles of plants. Conclusions The power cone is generated when the radial power growth rate is unequal to the length power growth rate. The power cascade model operates independently of the logarithmic spiral and is present throughout diverse biological systems. The power cascade provides a mechanistic basis for the generation of these pointed structures across the tree of life.
... In a similar vein, the contributions to this special issue illustrate that the study of developmental bias spans different biological domains (and thus implicates different fields): gene regulation (e.g., Hu et al., 2019), parthenogenesis (Galis & van Alphen, 2019), phenotypic plasticity (Draghi, 2019;Levis & Pfennig, 2019;Parsons et al., 2019;Uller et al., 2019), the morphology of extant and fossil species (Jablonski, 2019;Jackson, 2019), brain development (Finlay & Huang, 2019), symbiosis and interactions involving microbial species (Gilbert, 2019), development of the vertebrate skeleton (Kavanagh, 2019), and behavior, learning, and niche construction (Hu et al., 2019;Laland et al., 2019), among others. Some of the studies are experimental, some include field work, and others make primarily use of theory and computational simulation (Draghi, 2019;Hordijk & Altenberg, 2019). ...
Article
Throughout the recent history of research at the intersection of evolution and development, notions such as developmental constraint, evolutionary novelty, and evolvability have been prominent, but the term “developmental bias” has scarcely been used. And one may even doubt whether a unique and principled definition of bias is possible. I argue that the concept of developmental bias can still play a vital scientific role by means of setting an explanatory agenda that motivates investigation and guides the formulation of integrative explanatory frameworks. Less crucial is a definition that would classify patterns of phenotypic variation and unify variational patterns involving different traits and taxa as all being “bias.” Instead, what we should want is a concept that generates intellectual identity across various researchers, and that unites the diverse fields and approaches relevant to the study of developmental bias, from paleontology to behavioral biology. I point to some advantages of conducting research specifically under the label of “developmental bias,” compared with employing other, more common terms such as “evolvability.” Research Highlights • It may not be possible to arrive at a definition of developmental bias that classifies patterns of phenotypic variation involving different traits and taxa as all exhibiting “bias.” But such a classificatory definition is not needed. • The concept of developmental bias can play a vital role by setting an explanatory agenda that motivates research, provides intellectual identity across diverse fields and approaches investigating developmental bias, and coordinates the formation of integrative explanatory frameworks. • Although there are other, more widely used notions pertaining to the generation of phenotypic variation, such as “evolvability,” there are reasons for conducting research specifically under the label of “developmental bias.”
... Functional relationships involving anatomical and morphological transformation during the 'dinosaur-bird' transition are reasonably well documented. However, factors involved in such a long-term macroevolutionary trend are not only functional, but deeply developmentally regulated (Erwin, 2000;Gilbert et al., 1996;Jablonski, 2020;Xu et al., 2014). Thus, the underlying mechanisms involved in the transformation of a new functional module (evolutionary innovation), such as theropod wings, remain poorly understood. ...
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The dinosaurian origin of birds is one of the best documented events that palaeontology has contributed to the understanding of deep time evolution. This transition has been studied on multiple fossils using numerous multidisciplinary resources, including systematics, taxonomic, anatomical, morphological, biomechanical and molecular approaches. However, whereas deep time origins and phylogenetic relationships are robust, important nuances of this transition’s dynamics remain controversial. In particular, the fossil record of several maniraptoran groups clearly shows that aerial locomotion was developed before an ‘avialization’ (i.e., before the first divergence towards avialans), thus earlier than presumed. Although aspects as important as miniaturization and the acquisition of several anatomical and morphological modifications are key factors determining such evolutionary transition, understanding this macroevolutionary trend also involves to seize the evolution of developmental systems, which requires assessing the morphological expression of integration and modularity of the locomotor apparatus throughout time. This is so because, as it happened in other flying vertebrate taxa such as pterosaurs and bats, the transformation of the maniraptoran forelimbs into flying locomotor modules must not only have involved a gradual anatomical transformation, but also a complete developmental re-patterning of the integration scheme between them and the hindlimbs. Here, we review the most relevant aspects of limb morphological transformation during the so-called ‘dinosaur-bird’ transition to stress the importance of assessing the role of modularity and morphological integration in such macroevolutionary transition, which ultimately involves the origins of flight in dinosaurs.
... Our study demonstrates that development can bias the evolutionary independence of traits, but it also shows how bias can be released through developmental innovations, thus, allowing rapid morphological change, facilitating evolutionary diversification. evolutionary biology | developmental biology | developmental bias T he developmental mechanisms that generate morphology can, in theory, bias the independent evolution of traits sharing ontogenetic pathways, making certain evolutionary changes less likely than others (1)(2)(3)(4)(5)(6)(7)(8). Eyespots are concentric circular markings, often with contrasting colors, that are found on the wings of many Lepidoptera (9)(10)(11). ...
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Development can bias the independent evolution of traits sharing ontogenetic pathways, making certain evolutionary changes less likely. The eyespots commonly found on butterfly wings each have concentric rings of differing colors, and these serially repeated pattern elements have been a focus for evo-devo research. In the butterfly family Nymphalidae, eyespots have been shown to function in startling or deflecting predators and to be involved in sexual selection. Previous work on a model species of Mycalesina butterfly, Bicyclus anynana, has provided insights into the developmental control of the size and color composition of individual eyespots. Experimental evolution has also shown that the relative size of a pair of eyespots on the same wing surface is highly flexible, whereas they are resistant to diverging in color composition, presumably due to the underlying shared developmental process. This fixed color composition has been considered as a prime example of developmental bias with significant consequences for wing pattern evolution. Here, we test this proposal by surveying eyespots across the whole subtribe of Mycalesina butterflies and demonstrate that developmental bias shapes evolutionary diversification except in the genus Heteropsis which has gained independent control of eyespot color composition. Experimental manipulations of pupal wings reveal that the bias has been released through a novel regional response of the wing tissue to a conserved patterning signal. Our study demonstrates that development can bias the evolutionary independence of traits, but it also shows how bias can be released through developmental innovations, thus, allowing rapid morphological change, facilitating evolutionary diversification.
... The fact that an organism's developmental systems are incapable of generating phenotypic variation equally in all directions, and therefore impose directionality on the trajectory of evolution, is by now well-accepted (Jablonski, 2020;Salazar-Cuidad, 2021). In plants, work on this concept of developmental constraint (and the inter-related concepts of developmental bias and developmental drive) have been extensive-ranging from studies on the evolution of floral organs (Wessinger and Hileman, 2016) to the role that it may play in structuring defenses to herbivores and pathogens during a plant's life cycle (Boege and Marquis, 2005)-and parallels work done in animals. ...
... Further, our data should be considered a ''presence-only'' dataset rather than presence-absence. There is a precedent within the paleontological literature for inferring trait evolution using phylogenetic comparative methods that use either presence-only datasets or datasets with unclear patterns of trait absence (e.g., Finarelli and Flynn, 2006;Benton, 2015;Hunt and Slater, 2016), particularly where appropriate trait data may be limited, such as behavior (Hsieh and Plotnick, 2020), physiology (e.g., Legendre et al., 2016), or development (Organ et al., 2015;Jablonski, 2020). Our method for the ability to infer the identity of non-soniferous families offers an opportunity to further explore these families for the potential of soniferous behavior. ...
... Further, our data should be considered a ''presence-only'' dataset rather than presence-absence. There is a precedent within the paleontological literature for inferring trait evolution using phylogenetic comparative methods that use either presence-only datasets or datasets with unclear patterns of trait absence (e.g., Finarelli and Flynn, 2006;Benton, 2015;Hunt and Slater, 2016), particularly where appropriate trait data may be limited, such as behavior (Hsieh and Plotnick, 2020), physiology (e.g., Legendre et al., 2016), or development (Organ et al., 2015;Jablonski, 2020). Our method for the ability to infer the identity of non-soniferous families offers an opportunity to further explore these families for the potential of soniferous behavior. ...
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Sound production by fishes has been recognized for millennia, but is typically regarded as comparatively rare and thus yet to be integrated into broader concepts of vertebrate evolution. We map the most comprehensive dataset of sound production yet assembled onto a family-level phylogeny of ray-finned fishes (Actinopterygii), a clade containing more than 34,000 extant species. Family-, rather than species-, level analyses allowed broad investigation of sound production mostly based on illustrations of acoustic recordings and morphological specializations (82%) strongly indicative of sound production along with qualitative descriptions (18%), and a conservative estimate of the distribution and ancestry of a character that is likely more widespread than currently known. Compilation of sonicrelated morphological characters shows 60 families exhibiting muscles coupled to swim bladder vibration and 39 families that employ movement of skeletal parts against each other, i.e., stridulation. Eighteen of these families, mostly catfishes (13), include individual species exhibiting both mechanisms. The results show that families with soniferous species contain nearly two-thirds of actinopterygian species, including a clade originating circa 155 Ma, and that sound production has independently evolved approximately 33 times within Actinopterygii. Despite the uncertainties of presence-only data records and incomplete evidence of absence, under-sampling species, and assuming family-level conservation of sound production, sensitivity analyses show that these patterns of shared ancestry are robust. In aggregate, these findings offer a new perspective on the ancestry and convergent evolution of sound production among actinopterygians, a clade representing more than half of extant vertebrate species.
... Clustering in morphospace can also suggest a developmental constraint (Jablonski, 2020) that impedes species to change their traits after speciation (Pie & Weitz, 2005). Given that saltwater species are fully nested within the shape space of freshwater ones, it suggests that apparently the shape of RBC of saltwater species is more constrained than freshwater ones. ...
Article
The size and shape of Red Blood Cells (RBC) provide key information on life history strategies in vertebrates. However, little is known about how RBC shape evolved in response to environmental factors, body size, and the role of evolutionary rate. Here, we analyzed RBC morphometrics in a set of Teleostei (bony fishes) and Elasmobranchii (sharks and rays) species testing the hypothesis that phylogenetic relationship explains species occupation of morphospace. We collected data on cell and nucleus area and volume, nucleus:cytoplasm ratio, and shape factor for 65 species belonging to 28 orders. Then, we built phylomorphospaces separately for bony fish and sharks and rays. To test if phylogenetic relationships predicted phenotypic similarity, we calculated multivariate phylogenetic signal. We also estimated the evolutionary rate of RBC shape for each node and tip using ridge regression. Finally, we tested if habitat and body size influenced RBC shape using a PGLS. We found a significant phylogenetic signal in RBC shape for bony fish, but not sharks and rays. Saltwater teleost species were more clustered than freshwater ones in the phylomorphospace, suggesting clade disparity. Accordingly, the rate of evolution was highly heterogeneous, with significant decrease in Acanthopterygii. Neither habitat nor body size influenced RBC shape. In conclusion, RBC shape seem to have evolved in fishes in response to multiple selective pressures independent of life history characters.
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Background Comparative morphology fundamentally relies on the orientation and alignment of specimens. In the era of geometric morphometrics, point-based homologies are commonly deployed to register specimens and their landmarks in a shared coordinate system. However, the number of point-based homologies commonly diminishes with increasing phylogenetic breadth. These situations invite alternative, often conflicting, approaches to alignment. The bivalve shell (Mollusca: Bivalvia) exemplifies a homologous structure with few universally homologous points—only one can be identified across the Class, the shell ‘beak’. Here, we develop an axis-based framework, grounded in the homology of shell features, to orient shells for landmark-based, comparative morphology. Methods Using 3D scans of species that span the disparity of shell morphology across the Class, multiple modes of scaling, translation, and rotation were applied to test for differences in shell shape. Point-based homologies were used to define body axes, which were then standardized to facilitate specimen alignment via rotation. Resulting alignments were compared using pairwise distances between specimen shapes as defined by surface semilandmarks. Results Analysis of 45 possible alignment schemes finds general conformity among the shape differences of ‘typical’ equilateral shells, but the shape differences among atypical shells can change considerably, particularly those with distinctive modes of growth. Each alignment corresponds to a hypothesis about the ecological, developmental, or evolutionary basis of morphological differences, but we suggest orientation via the hinge line for many analyses of shell shape across the Class, a formalization of the most common approach to morphometrics of shell form. This axis-based approach to aligning specimens facilitates the comparison of approximately continuous differences in shape among phylogenetically broad and morphologically disparate samples, not only within bivalves but across many other clades.
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The term 'developmental bias' promoted in the Special Issue of ‘Evolution & Development’ was initially defined as the effect in evolution direction creating by correlation of changed developmental parameters. The understanding of the term is in the Special Issue much broader and very poorly defined. Promoting such a broad term related to observation makes difficult to explain specific mechanisms. It is now time for the task of explaining to become more important in biology than just collecting facts. The term requires quick organization and division into many different concepts. I suggest replacing this term with a shorter one (devbias) with an additional tip indicating a specific variant according to the proposed ordering system. Mainly the mechanisms giving variability clearly focused on greater fitness (devbiases4) have been added. Devbias4 was treated in Special Issue as an independent source of adaptation supporting natural selection. Focusing on the time interval of current evolution, where collected devbiases4 indeed supports natural selection, it is usually forgotten to stress that they are also the result of previous natural selection and only mediate the transmission of its effects. This leads to a dangerous message beyond biology that scientific observations have shown that the Darwinian mechanism is not the only source of adaptation. By the way of ordering ‘devbias’ the understanding of ‘randomness’ is discussed to show differences between ‘flat distribution’, ‘variation blind on needs’ and ‘real random variability’ which in Special Issue are typically mixed.
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The concept of evolvability—the capacity of a population to produce and maintain evolutionarily relevant variation—has become increasingly prominent in evolutionary biology. Although paleontology has a long history of investigating questions of evolvability, often invoking different but allied terminology, the study of evolvability in the fossil record has seemed intrinsically problematic. How can we surmount difficulties in disentangling whether the causes of evolutionary patterns arise from variational properties of traits or lineages rather than due to selection and ecological success? Despite these challenges, the fossil record is unique in offering growing sources of data that span millions of years and therefore capture evolutionary patterns of sustained duration and significance otherwise inaccessible to evolutionary biologists. Additionally, there are a variety of strategic possibilities for combining prominent neontological approaches to evolvability with those from paleontology. We illustrate three of these possibilities with quantitative genetics, evolutionary developmental biology, and phylogenetic models of macroevolution. In conclusion, we provide a methodological schema that focuses on the conceptualization, measurement, and testing of hypotheses to motivate and provide guidance for future empirical and theoretical studies of evolvability in the fossil record.
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Modular evolution, the relatively independent evolution of body parts, may promote high morphological disparity in a clade. Conversely, integrated evolution via stronger covariation of parts may limit disparity. However, integration can also promote high disparity by channelling morphological evolution along lines of least resistance—a process that may be particularly important in the accumulation of disparity in the many invertebrate systems having accretionary growth. We use a time-calibrated phylogenetic hypothesis and high-density, three-dimensional semilandmarking to analyse the relationship between modularity, integration and disparity in the most diverse extant bivalve family: the Veneridae. In general, venerids have a simple, two-module parcellation of their body that is divided into features of the calcium carbonate shell and features of the internal soft anatomy. This division falls more along developmental than functional lines when placed in the context of bivalve anatomy and biomechanics. The venerid body is tightly integrated in absolute terms, but disparity appears to increase with modularity strength among subclades and ecologies. Thus, shifts towards more mosaic evolution beget higher morphological variance in this speciose family.
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On the basis of findings from developmental biology, some researchers have argued that evolutionary theory needs to be significantly updated. Advocates of such a “developmental update” have, among other things, suggested that we need to re-conceptualize units of selection, that we should expand our view of inheritance to include environmental as well as genetic and epigenetic factors, that we should think of organisms and their environment as involved in reciprocal causation, and that we should reevaluate the rates of evolutionary change. However, many of these same conclusions could be reached on the basis of other evidence, namely from microbiology. In this paper, I ask why microbiological evidence has not had a similarly large influence on calls to update biological theory, and argue that there is no principled reason to focus on developmental as opposed to microbiological evidence in support of these revisions to evolutionary theory. I suggest that the focus on developmental biology is more likely attributable to historical accident. I will also discuss some possible room for overlap between developmental and microbiology, despite the historical separation of these two subdisciplines.
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Mammal tooth morphology and function correlate strongly with dietary ecology, and convergence is a major feature of mammalian tooth evolution. Yet, function and ecology are insufficient to explain morphological diversification and convergence within mammalian molar evolution; suggesting that development and phylogeny also limit possible structural solutions to selective pressures. Here, I use in silico models and empirical studies of extant and fossil rodent teeth to identify morphogenetic rules that influence molar morphology. Because rodents are the most diverse group of mammals with corresponding dental disparity they represent an excellent system for investigating how genetic interactions limit morphology. I find that lower first molars are limited to a minimum of four cusps and a maximum of nine cusps. Multiple developmental pathways produce the same numbers of cusps, despite highly variable cusp morphologies, indicating the existence of limits on how morphological evolution can fill a morphospace defined by cusp numbers. These constraints are both developmental and phylogenetic in nature and the identification of their influence on rodent molar shape provides a framework for investigation of how tooth batteries evolved an array of functions despite fundamental structural limits. The data presented here increase predictability of cusp number and evolutionary outcomes of rodent cheek dentition.
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The radiation of mammals after the Cretaceous/Palaeogene (K/Pg) boundary was a major event in the evolution of terrestrial ecosystems. Multiple studies point to increases in maximum body size and body size disparity, but patterns of disparity for other traits are less clear owing to a focus on different indices and subclades. We conducted an inclusive comparison of jaw functional disparity from the Early Jurassic-latest Eocene, using six mechanically relevant mandibular ratios for 256 species representing all major groups. Jaw functional disparity across all mammals was low throughout much of the Mesozoic and remained low across the K/Pg boundary. Nevertheless, the K/Pg boundary was characterized by a pronounced pattern of turnover and replacement, entailing a substantial reduction of non-therian and stem-therian disparity, alongside a marked increase in that of therians. Total mammal disparity exceeded its Mesozoic maximum for the first time during the Eocene, when therian mammals began exploring previously unoccupied regions of function space. This delay in the rise of jaw functional disparity until the Eocene probably reflects the duration of evolutionary recovery after the K/Pg mass extinction event. This contrasts with the more rapid expansion of maximum body size, which occurred in the Palaeocene.
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A fundamental aim of post-genomic 21st century biology is to understand the genotype-phenotype map (GPM) or how specific genetic variation relates to specific phenotypic variation. Quantitative genetics approximates such maps using linear models, and has developed methods to predict the response to selection in a population. The other major field of research concerned with the GPM, developmental evolutionary biology or evo-devo, has found the GPM to be highly nonlinear and complex. Here we quantify how the predictions of quantitative genetics are affected by the complex, nonlinear maps found in developmental biology. We combine a realistic development-based GPM model and a population genetics model of recombination, mutation and natural selection. Each individual in the population consists of a genotype and a multi-trait phenotype that arises through the development model. We simulate evolution by applying natural selection on multiple traits per individual. In addition, we estimate the quantitative genetics parameters required to predict the response to selection. We found that the disagreements between predicted and observed responses to selection are common, roughly in a third of generations, and are highly dependent on the traits being selected. These disagreements are systematic and related to the nonlinear nature of the genotype-phenotype map. Our results are a step towards integrating the fields studying the GPM.
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Complexity in how mechanistic variation translates into ecological novelty could be critical to organismal diversification. For instance, when multiple distinct morphologies can generate the same mechanical or functional phenotype, this could mitigate trade-offs and/or provide alternative ways to meet the same ecological challenge. To investigate how this type of complexity shapes diversity in a classic adaptive radiation, we tested several evolutionary consequences of the anterior jaw four-bar linkage for Lake Malawi cichlid trophic diversification. Using a novel phylogenetic framework, we demonstrated that different mechanical outputs of the same four jaw elements are evolutionarily associated with both jaw protrusion distance and jaw protrusion angle. However, these two functional aspects of jaw protrusion have evolved independently. Additionally, although four-bar morphology showed little evidence for attraction to optima, there was substantial evidence of adaptive peaks for emergent four-bar linkage mechanics and jaw protrusion abilities among Malawi feeding guilds. Finally, we highlighted a clear case of two cichlid species that have independently evolved to graze algae in less than 2 Myr and have converged on similar jaw protrusion abilities as well as four-bar linkage mechanics, but have evolved these similarities via non-convergent four-bar morphologies. © 2019 The Author(s) Published by the Royal Society. All rights reserved.
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Understanding phenotypic diversification and the conditions that spur morphological novelty or constraint is a major theme in evolutionary biology. Unequal morphological diversity between sister clades can result from either differences in the rate of morphological change or in the ability of clades to explore novel phenotype ranges. We combine an existing phylogenetic framework with new phylogenomic data and geometric morphometrics to explore the relative roles of rate versus mode of morphological evolution for a hyperdiverse group: cryptine ichneumonid wasps. Data from genomic ultraconserved elements confirm that cryptines are divided into two large clades: one specialized in the use of hosts that are deeply concealed under hard substrates, and another with a much more diversified host range. Using a phylomorphospace approach, we show that both clades have experienced similar rates of morphological evolution. Nonetheless, the more specialized group is much more restricted in morphospace occupation, indicating that it repeatedly evolved morphological change through the same morphospace regions. This is in agreement with our prediction that host use imposes constraints in the morphospace available to lineages, and reinforces an important distinction between evolutionary stasis as opposed to a scenario of continual morphological change restricted to a certain range of morphotypes.
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Sharks of Late Paleozoic oceans evolved unique dentitions for catching and eating soft bodied prey. A diverse but poorly preserved clade, edestoids are noted for developing biting teeth at the midline of their jaws. Helicoprion has a continuously growing root to accommodate more than 100 crowns that spiraled on top of one another to form a symphyseal whorl supported and laterally braced within the lower jaw. Reconstruction of jaw mechanics shows that individual serrated crowns grasped, sliced, and pulled prey items into the esophagus. A new description and interpretation of Edestus provides insight into the anatomy and functional morphology of another specialized edestoid. Edestus has opposing curved blades of teeth that are segmented and shed with growth of the animal. Set on a long jaw the lower blade closes with a posterior motion, effectively slicing prey across multiple opposing serrated crowns. Further examples of symphyseal whorls among Edestoidae are provided from previously undescribed North American examples of Toxoprion, Campyloprion, Agassizodus, and Sinohelicoprion. The symphyseal dentition in edestoids is associated with a rigid jaw suspension and may have arisen in response to an increase in pelagic cephalopod prey during the Late Paleozoic. This article is protected by copyright. All rights reserved.
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Phenotypic integration and modularity are ubiquitous features of complex organisms, describing the magnitude and pattern of relationships among biological traits. A key prediction is that these relationships, reflecting genetic, developmental, and functional interactions, shape evolutionary processes by governing evolvability and constraint. Over the last 60 years, a rich literature of research has quantified patterns of integration and modularity across a variety of clades and systems. Only recently has it become possible to contextualize these findings in a phylogenetic framework to understand how trait integration interacts with evolutionary tempo and mode. Here, we review the state of macroevolutionary studies of integration and modularity, synthesizing empirical and theoretical work into a conceptual framework for predicting the effects of integration on evolutionary rate and disparity: a fly in a tube. While magnitude of integration is expected to influence the potential for phenotypic variation to be produced and maintained, thus defining the shape and size of a tube in morphospace, evolutionary rate, or the speed at which a fly moves around the tube, is not necessarily controlled by trait interactions. Finally, we demonstrate this reduced disparity relative to the Brownian expectation for a given rate of evolution with an empirical example: the avian cranium. This article is protected by copyright. All rights reserved
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We review the evolutionary importance of developmental mechanisms in constraining evolutionary changes in animals—in other words, developmental constraints. We focus on hard constraints that can act on macroevolutionary timescales. In particular, we discuss the causes and evolutionary consequences of the ancient metazoan constraint that differentiated cells cannot divide and constraints against changes of phylotypic stages in vertebrates and other higher taxa. We conclude that in all cases these constraints are caused by complex and highly controlled global interactivity of development, the disturbance of which has grave consequences. Mutations that affect such global interactivity almost unavoidably have many deleterious pleiotropic effects, which will be strongly selected against and will lead to long-term evolutionary stasis. The discussed developmental constraints have pervasive consequences for evolution and critically restrict regeneration capacity and body plan evolution. 499
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Transformations in morphology, physiology and behaviour along the mammalian stem lineage were accompanied by profound modifications to reproduction and growth, including the emergence of a reproductive strategy characterized by high maternal investment in a small number of offspring1,2 and heterochronic changes in early cranial development associated with the enlargement of the brain3. Because direct fossil evidence of these transitions is lacking, the timing and sequence of these modifications are unknown. Here we present what is, to our knowledge, the first fossil record of pre- or near-hatching young of any non-mammalian synapsid. A large clutch of well-preserved perinates of the tritylodontid Kayentatherium wellesi (Cynodontia, Mammaliamorpha) was found with a presumed maternal skeleton in Early Jurassic sediments of the Kayenta Formation. The single clutch comprises at least 38 individuals, well outside the range of litter sizes documented in extant mammals. This discovery confirms that production of high numbers of offspring represents the ancestral condition for amniotes, and also constrains the timing of a reduction in clutch size along the mammalian stem. Although tiny, the perinates have an overall skull shape that is similar to that of adults, with no allometric lengthening of the face during ontogeny. The only positive allometries are associated with the bones that support the masticatory musculature. Kayentatherium diverged just before a hypothesized pulse of brain expansion that reorganized cranial architecture at the base of Mammaliaformes4-6. The association of a high number of offspring and largely isometric cranial growth in Kayentatherium is consistent with a scenario in which encephalization-and attendant shifts in metabolism and development7,8-drove later changes to mammalian reproduction.
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The influence of biomechanics on the tempo and mode of morphological evolution is unresolved, yet is fundamental to organismal diversification. Across multiple four-bar linkage systems in animals, we discovered that rapid morphological evolution (tempo) is associated with mechanical sensitivity (strong correlation between a mechanical system's output and one or more of its components). Mechanical sensitivity is explained by size: the smallest link(s) are disproportionately affected by length changes and most strongly influence mechanical output. Rate of evolutionary change (tempo) is greatest in the smallest links and trait shifts across phylogeny (mode) occur exclusively via the influential, small links. Our findings illuminate the paradigms of many-to-one mapping, mechanical sensitivity, and constraints: tempo and mode are dominated by strong correlations that exemplify mechanical sensitivity, even in linkage systems known for exhibiting many-to-one mapping. Amidst myriad influences, mechanical sensitivity imparts distinct, predictable footprints on morphological diversity.
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A recurrent theme in evolutionary biology is to contrast natural selection and developmental constraint – two forces pitted against each other as competing explanations for organismal form. Despite its popularity, this juxtaposition is deeply misleading.... Phenotypic variation is generated by the processes of development, with some variants arising more readily than others—a phenomenon known as “developmental bias.” Developmental bias and natural selection have often been portrayed as alternative explanations, but this is a false dichotomy: developmental bias can evolve through natural selection, and bias and selection jointly influence phenotypic evolution. Here, we briefly review the evidence for developmental bias and illustrate how it is studied empirically. We describe recent theory on regulatory networks that explains why the influence of genetic and environmental perturbation on phenotypes is typically not uniform, and may even be biased toward adaptive phenotypic variation. We show how bias produced by developmental processes constitutes an evolving property able to impose direction on adaptive evolution and influence patterns of taxonomic and phenotypic diversity. Taking these considerations together, we argue that it is not sufficient to accommodate developmental bias into evolutionary theory merely as a constraint on evolutionary adaptation. The influence of natural selection in shaping developmental bias, and conversely, the influence of developmental bias in shaping subsequent opportunities for adaptation, requires mechanistic models of development to be expanded and incorporated into evolutionary theory. A regulatory network perspective on phenotypic evolution thus helps to integrate the generation of phenotypic variation with natural selection, leaving evolutionary biology better placed to explain how organisms adapt and diversify.
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Morphological homeostasis limits the extent to which genetic and/or environmental variation is translated into phenotypic variation, providing generation-to-generation fitness advantage under a stabilizing selection regime. Depending on its lability, morphological homeostasis might also have a longer-term impact on evolution by restricting the variation-and thus the response to directional selection-of a trait. The fossil record offers an inviting opportunity to investigate whether and how morphological homeostasis constrained trait evolution in lineages or clades on long timescales (thousands to millions of years) that are not accessible to neontological studies. Fossils can also reveal insight into the nature of primitive developmental systems that might not be predictable from the study of modern organisms. The ability to study morphological homeostasis in fossils is strongly limited by taphonomic processes that can destroy, blur, or distort the original biological signal: genetic data are unavailable; phenotypic data can be modified by tectonic or compaction-related deformation; time-averaging limits temporal resolution; and environmental variation is hard to study and impossible to control. As a result of these processes, neither allelic sensitivity (and thus genetic canalization) nor macroenvironmental sensitivity (and thus environmental canalization) can be unambiguously assessed in the fossil record. However, homeorhesis-robustness against microenvironmental variation (developmental noise)-can be assessed in ancient developmental systems by measuring the level of fluctuating asymmetry (FA) in a nominally symmetric trait. This requires the analysis of multiple, minimally time-averaged samples of exquisite preservational quality. Studies of FA in fossils stand to make valuable contributions to our understanding of the deep-time significance of homeorhesis. Few empirical studies have been conducted to date, and future paleontological research focusing on how homeorhesis relates to evolutionary rate (including stasis), species survivorship, and purported macroevolutionary trends in evolvability would reap high reward.
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Time-calibrated phylogenies of living species have been widely used to study the tempo and mode of species diversification. However, it is increasingly clear that inferences about species diversification - extinction rates in particular - can be unreliable in the absence of paleontological data. We introduce a general framework based on the fossilized birth-death process for studying speciation-extinction dynamics on phylogenies of extant and extinct species. The model assumes that phylogenies can be modeled as a mixture of distinct evolutionary rate regimes and that a hierarchical Poisson process governs the number of such rate regimes across a tree. We implemented the model in BAMM, a computational framework that uses reversible jump Markov chain Monte Carlo to simulate a posterior distribution of macroevolutionary rate regimes conditional on the branching times and topology of a phylogeny. The implementation we describe can be applied to paleontological phylogenies, neontological phylogenies, and to phylogenies that include both extant and extinct taxa. We evaluate performance of the model on datasets simulated under a range of diversification scenarios. We find that speciation rates are reliably inferred in the absence of paleontological data. However, the inclusion of fossil observations substantially increases the accuracy of extinction rate estimates. We demonstrate that inferences are relatively robust to at least some violations of model assumptions, including heterogeneity in preservation rates and misspecification of the number of occurrences in paleontological datasets.
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Modularity is considered a prerequisite for the evolvability of biological systems. This is because in theory, individual modules can follow quasi-independent evolutionary trajectories or evolve at different rates compared to other aspects of the organism. This may influence the potential of some modules to diverge, leading to differences in disparity. Here, we investigated this relationship between modularity, rates of morphological evolution and disparity using a phylogenetically diverse sample of ray-finned fishes. We compared the support for multiple hypotheses of evolutionary modularity and asked if the partitions delimited by the best-fitting models were also characterized by the highest evolutionary rate differentials. We found that an evolutionary module incorporating the dorsal, anal and paired fins was well supported by the data, and that this module evolves more rapidly and consequently generates more disparity than other modules. This suggests that modularity may indeed promote morphological disparity through differences in evolutionary rates across modules. www.nature.com/articles/s41598-018-25715-y
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How traits influence species persistence is a fundamental question in ecology, evolution and palaeontology. We test the relationship between dietary traits and both species duration and locality coverage over 40 million years in North American canids, a clade with considerable ecomorphological disparity and a dense fossil record. Because ecomorphological generalization—broad resource use—may enable species to withstand disturbance, we predicted that canids of average size and mesocarnivory would exhibit longer durations and wider distributions than specialized larger or smaller species. Second, because locality coverage might reflect dispersal ability and/or survivability in a range of habitats, we predicted that high coverage would correspond with longer durations. We find a nonlinear relationship between species duration and degree of carnivory: species at either end of the carnivory spectrum tend to have shorter durations than mesocarnivores. Locality coverage shows no relationship with size, diet or duration. To test whether generalization (medium size, mesocarnivory) corresponds to an adaptive optimum, we fit trait evolution models to previously generated canid phylogenies. Our analyses identify no single optimum in size or diet. Instead, the primary model of size evolution is a classic Cope's Rule increase over time, while dietary evolution does not conform to a single model.
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The detailed anatomical features that characterize fossil hominin molars figure prominently in the reconstruction of their taxonomy, phylogeny, and paleobiology. Despite the prominence of molar form in human origins research, the underlying developmental mechanisms generating the diversity of tooth crown features remain poorly understood. A model of tooth morphogenesis—the patterning cascade model (PCM)—provides a developmental framework to explore how and why the varying molar morphologies arose throughout human evolution. We generated virtual maps of the inner enamel epithelium—an indelibly preserved record of enamel knot arrangement—in 17 living and fossil hominoid species to investigate whether the PCM explains the expression of all major accessory cusps. We found that most of the variation and evolutionary changes in hominoid molar morphology followed the general developmental rule shared by all mammals, outlined by the PCM. Our results have implications for the accurate interpretation of molar crown configuration in hominoid systematics.
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Mosaic evolution, which results from multiple influences shaping morphological traits and can lead to the presence of a mixture of ancestral and derived characteristics, has been frequently invoked in describing evolutionary patterns in birds. Mosaicism implies the hierarchical organization of organismal traits into semiautonomous subsets, or modules, which reflect differential genetic and developmental origins. Here, we analyze mosaic evolution in the avian skull using high-dimensional 3D surface morphometric data across a broad phylogenetic sample encompassing nearly all extant families. We find that the avian cranium is highly modular, consisting of seven independently evolving anatomical regions. The face and cranial vault evolve faster than other regions, showing several bursts of rapid evolution. Other modules evolve more slowly following an early burst. Both the evolutionary rate and disparity of skull modules are associated with their developmental origin, with regions derived from the anterior mandibular-stream cranial neural crest or from multiple embryonic cell populations evolving most quickly and into a greater variety of forms. Strong integration of traits is also associated with low evolutionary rate and low disparity. Individual clades are characterized by disparate evolutionary rates among cranial regions. For example, Psittaciformes (parrots) exhibit high evolutionary rates throughout the skull, but their close relatives, Falconiformes, exhibit rapid evolution in only the rostrum. Our dense sampling of cranial shape variation demonstrates that the bird skull has evolved in a mosaic fashion reflecting the developmental origins of cranial regions, with a semi-independent tempo and mode of evolution across phenotypic modules facilitating this hyperdiverse evolutionary radiation.
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Approaches to macroevolution require integration of its two fundamental components, within a hierarchical framework. Following a companion paper on the origin of variation, I here discuss sorting within an evolutionary hierarchy. Species sorting—sometimes termed species selection in the broad sense, meaning differential origination and extinction owing to intrinsic biological properties—can be split into strict-sense species selection, in which rate differentials are governed by emergent, species-level traits such as geographic range size, and effect macroevolution, in which rates are governed by organism-level traits such as body size; both processes can create hitchhiking effects, indirectly causing the proliferation or decline of other traits. Several methods can operationalize the concept of emergence, so that rigorous separation of these processes is increasingly feasible. A macroevolutionary tradeoff, underlain by the intrinsic traits that influence evolutionary dynamics, causes speciation and extinction rates to covary in many clades, resulting in evolutionary volatility of some clades and more subdued behavior of others; the few clades that break the tradeoff can achieve especially prolific diversification. In addition to intrinsic biological traits at multiple levels, extrinsic events can drive the waxing and waning of clades, and the interaction of traits and events are difficult but important to disentangle. Evolutionary trends can arise in many ways, and at any hierarchical level; descriptive models can be fitted to clade trajectories in phenotypic or functional spaces, but they may not be diagnostic regarding processes, and close attention must be paid to both leading and trailing edges of apparent trends. Biotic interactions can have negative or positive effects on taxonomic diversity within a clade, but cannot be readily extrapolated from the nature of such interactions at the organismic level. The relationships among macroevolutionary currencies through time (taxonomic richness, morphologic disparity, functional variety) are crucial for understanding the nature of evolutionary diversification. A novel approach to diversity-disparity analysis shows that taxonomic diversifications can lag behind, occur in concert with, or precede, increases in disparity. Some overarching issues relating to both the origin and sorting of clades and phenotypes include the macroevolutionary role of mass extinctions, the potential differences between plant and animal macroevolution, whether macroevolutionary processes have changed through geologic time, and the growing human impact on present-day macroevolution. Many challenges remain, but progress is being made on two of the key ones: (a) the integration of variation-generating mechanisms and the multilevel sorting processes that act on that variation, and (b) the integration of paleontological and neontological approaches to historical biology.
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Sewall Wright's fitness landscape introduced the concept of evolutionary spaces in 1932. George Gaylord Simpson modified this to an adaptive, phenotypic landscape in 1944 and since then evolutionary spaces have played an important role in evolutionary theory through fitness and adaptive landscapes, phenotypic and functional trait spaces, morphospaces and related concepts. Although the topology of such spaces is highly variable, from locally Euclidean to pre-topological, evolutionary change has often been interpreted as a search through a pre-existing space of possibilities, with novelty arising by accessing previously inaccessible or difficult to reach regions of a space. Here I discuss the nature of evolutionary novelty and innovation within the context of evolutionary spaces, and argue that the primacy of search as a conceptual metaphor ignores the generation of new spaces as well as other changes that have played important evolutionary roles. This article is part of the themed issue ‘Process and pattern in innovations from cells to societies’.
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To better understand the patterns and processes shaping large-scale phenotypic diversification, I integrate palaeobiological and phylogenetic perspectives to investigate a ~200-million-year radiation using a global sample of Palaeozoic crinoid echinoderms. Results indicate the early history of crinoid diversification is characterized by early burst dynamics with decelerating morphologic rates. However, in contrast with expectation for a single "early burst" model, morphospace continued to expand following a slowdown in rates. In addition, I find evidence for an isolated peak in morphologic rates occurring late in the clade's history. This episode of elevated rates is not associated with increased disparity, morphologic novelty, or the radiation of a single subclade. Instead, this episode of elevated rates involved multiple subclade radiations driven by environmental change toward a pre-existing adaptive optimum. The decoupling of morphologic disparity with rates of change suggests phenotypic rates are primarily shaped by ecologic factors rather than the origination of morphologic novelty alone. These results suggest phenotypic diversification is far more complex than models commonly assumed in comparative biology. Furthermore, palaeontological disparity patterns are not a reliable proxy for rates after an initial diversifying phase. These issues highlight the need for continued synthesis between fossil and phylogenetic approaches to macroevolution.
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Reconciling the origins of morphological diversity with the deep homology of underlying mechanisms is a question fundamental to the goals of evolutionary developmental biology ("evo-devo" or EDB). In this paper I argue that differing research agendas in evolutionary and developmental biology have hindered how we address this question, but that the limb provides ideal "common ground" for their fuller integration. To support this idea, I review two previous analyses of limb variation in mammal, bird, and reptile taxa that offer complementary approaches to explaining diversity. Specifically, I present evidence suggesting that: (1) a shared genetic architecture affects the pattern of between limb developmental integration, while their functional dissociation is linked to both increased phenotypic evolvability and diversity of interlimb proportions, and (2) within limb proportional diversity is biased such that proximal and distal segments function as tradeoffs while the middle segment is more conservative, a signal that is both evident from early in morphogenesis and suggestive of an "inhibitory cascade" model of limb proximo-distal axis development. In the first case, shared genetic mechanisms predict both observed developmental integration between limbs and patterns of clade-specific diversity. In the second case, underappreciated patterns of phenotypic diversity suggest novel insights into the underlying developmental mechanisms by which variation is generated. These studies show how insights from both evolutionary and developmental biology of the limb may be used to generate novel testable hypotheses into the origins of diversity that are broadly applicable to the integration of EDB.
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Evolutionary ecologists aim to explain and predict evolutionary change under different selective regimes. Theory suggests that such evolutionary prediction should be more difficult for biomechanical systems in which different trait combinations generate the same functional output: "many-to-one mapping". Many-to-one mapping of phenotype to function enables multiple morphological solutions to meet the same adaptive challenges. Therefore, many-to-one mapping should undermine parallel morphological evolution, and hence evolutionary predictability, even when selection pressures are shared among populations. Studying 16 replicate pairs of lake- and stream-adapted threespine stickleback (Gasterosteus aculeatus), we quantified three parts of the teleost feeding apparatus and used biomechanical models to calculate their expected functional outputs. The three feeding structures differed in their form-to-function relationship from one-to-one (lower jaw lever ratio) to increasingly many-to-one (buccal suction index, opercular 4-bar linkage). We tested for (1) weaker linear correlations between phenotype and calculated function, and (2) less parallel evolution across lake-stream pairs, in the many-to-one systems relative to the one-to-one system. We confirm both predictions, thus supporting the theoretical expectation that increasing many-to-one mapping undermines parallel evolution. Therefore, sole consideration of morphological variation within and among populations might not serve as a proxy for functional variation when multiple adaptive trait combinations exist. This article is protected by copyright. All rights reserved.
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Geometric morphometrics is widely used to study underlying causal factors in phenotypic evolution and to reconstruct evolutionary history of phenotypes. However, non-linearities in the phenotypic landscape may exist such that analytical solutions derived from comparison of phenotypes in morphospace may have complex or contradictory relationships in the space of the underlying factors. Ancestral reconstruction of horn morphology based on two mammalian ungulates illustrates how biologically improbable results can arise from the mathematical properties of geometric morphometric morphospaces. Raup's shell coiling equations are used to illustrate the potential for contradictory conclusions to be drawn from ancestral reconstructions in parameter spaces (such as measurements of levels of gene expression or allele frequencies) versus shape spaces (such as morphospaces based on phenotypic analysis). These examples are generalizable to many real morpho-metric studies, suggesting that care should be taken when drawing conclusions about genetic, developmental, or environmental processes based on morphometric analyses. Dense sampling of shape space and the use of fully multivariate and, perhaps, non-linear methods can help forestall potential problems.
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Approaches to macroevolution require integration of its two fundamental components, i.e. the origin and the sorting of variation, in a hierarchical framework. Macroevolution occurs in multiple currencies that are only loosely correlated, notably taxonomic diversity, morphological disparity, and functional variety. The origin of variation within this conceptual framework is increasingly understood in developmental terms, with the semi-hierarchical structure of gene regulatory networks (GRNs, used here in a broad sense incorporating not just the genetic circuitry per se but the factors controlling the timing and location of gene expression and repression), the non-linear relation between magnitude of genetic change and the phenotypic results, the evolutionary potential of co-opting existing GRNs, and developmental responsiveness to nongenetic signals (i.e. epigenetics and plasticity), all requiring modification of standard microevolutionary models, and rendering difficult any simple definition of evolutionary novelty. The developmental factors underlying macroevolution create anisotropic probabilities—i.e., an uneven density distribution—of evolutionary change around any given phenotypic starting point, and the potential for coordinated changes among traits that can accommodate change via epigenetic mechanisms. From this standpoint, “punctuated equilibrium” and “phyletic gradualism” simply represent two cells in a matrix of evolutionary models of phenotypic change, and the origin of trends and evolutionary novelty are not simply functions of ecological opportunity. Over long timescales, contingency becomes especially important, and can be viewed in terms of macroevolutionary lags (the temporal separation between the origin of a trait or clade and subsequent diversification); such lags can arise by several mechanisms: as geological or phylogenetic artifacts, or when diversifications require synergistic interactions among traits, or between traits and external events. The temporal and spatial patterns of the origins of evolutionary novelties are a challenge to macroevolutionary theory; individual events can be described retrospectively, but a general model relating development, genetics, and ecology is needed. An accompanying paper (Jablonski in Evol Biol 2017) reviews diversity dynamics and the sorting of variation, with some general conclusions.
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A charm of biology as a scientific discipline is the diversity of life. Although this diversity can make laws of biology challenging to discover, several repeated patterns and general principles govern evolutionary diversification. Convergent evolution, the independent evolution of similar phenotypes, has been at the heart of one approach to understand generality in the evolutionary process. Yet understanding when and why organismal traits and strategies repeatedly evolve has been a central challenge. These issues were the focus of the American Society of Naturalists Vice Presidential Symposium in 2016 and are the subject of this collection of articles. Although naturalists have long made inferences about convergent evolution and its importance, there has been confusion in the interpretation of the pattern of convergence. Does convergence primarily indicate adaptation or constraint? How often should convergence be expected? Are there general principles that would allow us to predict where and when...
Book
Today developmental and evolutionary biologists are focussing renewed attention on the developmental process--those genetic and cellular factors that influence variation in individual body shape or metabolism--in an attempt to better understand how evolutionary trends and patterns within individuals might be limited and controlled. In this important work, the author reviews the classical literature on embryology, morphogenesis, and paleontology, and presents recent genetic and molecular studies on development. The result is a unique perspective on a set of problems of fundamental importance to developmental and evolutionary biologists.
Article
A fundamental aim of post‐genomic 21st century biology is to understand the genotype‐phenotype map (GPM) or how specific genetic variation relates to specific phenotypic variation. Quantitative genetics approximates such maps using linear models, and has developed methods to predict the response to selection in a population. The other major field of research concerned with the GPM, developmental evolutionary biology or evo‐devo, has found the GPM to be highly nonlinear and complex. Here we quantify how the predictions of quantitative genetics are affected by a complex, nonlinear map based on the development of a multicellular organ. We compared the predicted change in mean phenotype for a single generation using the multivariate breeder's equation, with the change observed from the model of development. We found that there are frequent disagreements between predicted and observed responses to selection due to the nonlinear nature of the genotype‐phenotype map. Our results are a step towards integrating the fields studying the GPM. This article is protected by copyright. All rights reserved
Article
Extinct crocodyliforms from the age of dinosaurs (Mesozoic Era) display an impressive range of skeletal morphologies, suggesting a diversity of ecological roles not found in living representatives [1-6]. In particular, unusual dental morphologies develop repeatedly through the evolutionary history of this group [2, 4-9]. Recent descriptions of fossil crocodyliforms and their unusual teeth provide the inferential basis for a wide range of feeding ecologies. However, tests of these hypotheses are hindered by the lack of directly comparable dental morphologies in living reptiles and mammals, thereby preventing an accurate ecosystem reconstruction. Here, we demonstrate, using a combination of the orientation patch count rotated method and discrete morphological features, that Mesozoic crocodyliforms exploited a much greater range of feeding ecologies than their extant relatives, including likely omnivores and herbivores. These results also indicate that crocodyliforms independently developed high-complexity dentitions a minimum of three times. Some taxa possess teeth that surpass the complexities of living herbivorous lizards and rival those of omnivorous and herbivorous mammals. This study indicates that herbivorous crocodyliforms were more common than previously thought and were present throughout the Mesozoic and on most continents. The occurrence of multiple origins of complex dentitions throughout Crocodyliformes indicates that herbivory was a beneficial dietary strategy and not a unique occurrence. Many of these crocodyliforms lived alongside omnivorous or herbivorous synapsids, illustrating an ecological partition that is not observed today.
Article
Cretaceous clavagellid pelecypods are a poorly known group, and have previously received little study. Ascaulocardium armatum is conchologically the most complex burrowing pelecypod known. From the study of living clavagellids, it is possible to interpret the various tubes extending outward from the adventitious crypt of A. armatum as devices for hydraulic burrowing and deposit feeding. The conchologically complex A. armatum occurs near the beginning of the history of the Clavagellidae, and does not seem to have given rise to any younger species. Ascaulocardium armatum is known only from the Upper Cretaceous rocks (Santonian–Maastrichtian) of the east Gulf and Atlantic Coastal Plains of the United States of America, as is probably the genus Ascaulocardium . All known Cretaceous clavagellids are burrowing species having a free right valve, and this is the ancestral mode of life of the Clavagellidae. Clavagellids that have a boring habit are a more recent evolutionary development, as are burrowing species having both juvenile valves cemented to the crypt. Clavagellids probably evolved from Jurassic–Early Cretaceous pholadomyids. Almost all Cretaceous clavagellids occur outside the Tethyan Zoogeographic Realm; this distribution is in marked contrast to the modern distribution of the family. Living species mostly inhabit clear, shallow seas in subtropical to tropical shelf areas.
Article
Morphological transformations can be generated by evolutionary changes in the sequence of developmental events. In this study, we examined the evolutionary dynamics of the developmental sequence on a macroevolutionary scale in teleosts. Using the information from previous reports describing the development of 31 species, we extracted the developmental sequences of 19 landmark events involving the formation of phylogenetically conserved body parts; we then inferred ancestral developmental sequences by two different parsimony‐based methods—event‐pairing and continuous analysis. The phylogenetic comparisons of these sequences revealed event‐dependent heterogeneity in the frequency of sequence changes. Most of the sequence changes occurred as exchanges of temporally neighboring events. These heterochronic changes in developmental sequences accumulated along evolutionary time, but the precise distribution of the changes over the teleostean phylogeny remains unclear due to technical limitations.
Article
Trilobites are often considered exemplary for understanding the Cambrian explosion of animal life, due to their unsurpassed diversity and abundance. These biomineralized arthropods appear abruptly in the fossil record with an established diversity, phylogenetic disparity, and provincialism at the beginning of Cambrian Series 2 (∼521 Ma), suggesting a protracted but cryptic earlier history that possibly extends into the Precambrian. However, recent analyses indicate elevated rates of phenotypic and genomic evolution for arthropods during the early Cambrian, thereby shortening the phylogenetic fuse. Furthermore, comparatively little research has been devoted to understanding the duration of the Cambrian explosion, after which normal Phanerozoic evolutionary rates were established. We test these hypotheses by applying Bayesian tip-dating methods to a comprehensive dataset of Cambrian trilobites. We show that trilobites have a Cambrian origin, as supported by the trace fossil record and molecular clocks. Surprisingly, they exhibit constant evolutionary rates across the entire Cambrian, for all aspects of the preserved phenotype: discrete, meristic, and continuous morphological traits. Our data therefore provide robust, quantitative evidence that by the time the typical Cambrian fossil record begins (∼521 Ma), the Cambrian explosion had already largely concluded. This suggests that a modern-style marine biosphere had rapidly emerged during the latest Ediacaran and earliest Cambrian (∼20 million years), followed by broad-scale evolutionary stasis throughout the remainder of the Cambrian.
Article
The measurement of morphological variation in macroevolutionary studies is increasingly based on morphospaces constructed from discrete character data. This trend mostly results from the appropriation of phylogenetic data matrices as character spaces for carrying out disparity analyses. Phylogenetic matrices provide morphological descriptions of taxa as combinations of character states and thus appear, if not conceptually, at least mathematically, comparable to discrete character datasets found in numerical taxonomy or built for disparity purposes. Hence, phylogenetic matrices seem to constitute an abundant source of data readily available for morphospace analyses. Discrete character spaces have generally been described as more flexible than morphospaces capturing continuous shape variation. The discrete coding of morphology allows morphospaces to accommodate more disparate morphologies and the ability of discrete character schemes to handle missing data is also often emphasized. This flexibility comes at a cost, however. Multivariate ordinations of such spaces often provide deceptive visualizations and may invite the use of inappropriate methodologies for their exploration. The large amount of missing data that typifies many phylogenetic datasets is also problematic for the measurement of dissimilarity among taxa and can therefore be detrimental to the assessment of morphological disparity. Here, the properties of discrete character spaces are described and common pitfalls discussed. Graphical and methodological approaches are suggested to circumvent or limit their impact, and greater caution is recommended when using discrete character data for morphospace and disparity inferences.
Article
'Early bursts' of morphological disparity (i.e. diversity of anatomical types) are common in the fossil record. We typically model such bursts as elevated early rates of independent character change. Developmental theory predicts that modules of linked characters can change together, which would mimic the effects of elevated independent rates on disparity. However, correlated change introducing suboptimal states should encourage breakup (parcellation) of character suites allowing new (or primitive) states to evolve until new suites arise (relinkage). Thus, correlated change-breakup-relinkage presents mechanisms for early bursts followed by constrained evolution. Here, I analyse disparity in 257 published character matrices of fossil taxa. For each clade, I use inverse-modelling to infer most probably rates of independent change given both time-homogeneous and separate 'early versus late' rates. These rates are used to estimate expected disparity given both independent change models. The correlated change-breakup-relinkage model also predicts elevated frequencies of compatible character state-pairs appearing out of order in the fossil record (e.g. 01 appearing after 00 and 11; = low stratigraphic compatibility), as one solution to suboptimal states induced by correlated change is a return to states held before that change. As predicted by the correlated change-breakup-relinkage model, early disparity in the majority of clades both exceeds the expectations of either independent change model and excess early disparity correlates with low stratigraphic compatibility among character-pairs. Although it is possible that other mechanisms for linking characters contribute to these patterns, these results corroborate the idea that reorganization of developmental linkages is often associated with the origin of groups that biologists recognize as new higher taxa and that such reorganization offers a source of new disparity throughout the Phanerozoic.
Article
Historical processes display some degree of “contingency,” meaning their outcomes are sensitive to seemingly inconsequential events that can fundamentally change the future. Contingency is what makes historical outcomes unpredictable. Unlike many other natural phenomena, evolution is a historical process. Evolutionary change is often driven by the deterministic force of natural selection, but natural selection works upon variation that arises unpredictably through time by random mutation, and even beneficial mutations can be lost by chance through genetic drift. Moreover, evolution has taken place within a planetary environment with a particular history of its own. This tension between determinism and contingency makes evolutionary biology a kind of hybrid between science and history. While philosophers of science examine the nuances of contingency, biologists have performed many empirical studies of evolutionary repeatability and contingency. Here, we review the experimental and comparative evidence from these studies. Replicate populations in evolutionary “replay” experiments often show parallel changes, especially in overall performance, although idiosyncratic outcomes show that the particulars of a lineage’s history can affect which of several evolutionary paths is taken. Comparative biologists have found many notable examples of convergent adaptation to similar conditions, but quantification of how frequently such convergence occurs is difficult. On balance, the evidence indicates that evolution tends to be surprisingly repeatable among closely related lineages, but disparate outcomes become more likely as the footprint of history grows deeper. Ongoing research on the structure of adaptive landscapes is providing additional insight into the interplay of fate and chance in the evolutionary process.
Article
Ancestral vertebrate habitats are subject to controversy and obscured by limited, often contradictory paleontological data. We assembled fossil vertebrate occurrence and habitat datasets spanning the middle Paleozoic (480 million to 360 million years ago) and found that early vertebrate clades, both jawed and jawless, originated in restricted, shallow intertidal-subtidal environments. Nearshore divergences gave rise to body plans with different dispersal abilities: Robust fishes shifted shoreward, whereas gracile groups moved seaward. Fresh waters were invaded repeatedly, but movement to deeper waters was contingent upon form and short-lived until the later Devonian. Our results contrast with the onshore-offshore trends, reef-centered diversification, and mid-shelf clustering observed for benthic invertebrates. Nearshore origins for vertebrates may be linked to the demands of their mobility and may have influenced the structure of their early fossil record and diversification.
Article
The evolutionary diversification of birds has been facilitated by specializations for various locomotor modes, with which the proportion of the limb skeleton is closely associated. However, recent studies have identified phylogenetic signals in this system, suggesting the presence of historical factors that have affected its evolutionary variability. In this study, in order to explore potential roles of ontogenetic integration in biasing the evolution in the avian limb skeleton, evolutionary diversification patterns in six avian families (Anatidae, Procellariidae, Ardeidae, Phalacrocoracidae, Laridae, and Alcidae) were examined and compared to the postnatal ontogenetic trajectories in those taxa, based on measurement of 2641 specimens and recently collected ontogenetic series, supplemented by published data. Morphometric analyses of lengths of six limb bones (humerus, ulna, carpometacarpus, femur, tibiotarsus, and tarsometatarsus) demonstrated that: 1) ontogenetic trajectories are diverse among families; 2) evolutionary diversification is significantly anisotropic; and, most importantly, 3) major axes of evolutionary diversification are correlated with clade‐specific ontogenetic major axes in the shape space. These results imply that the evolutionary variability of the avian limbs has been biased along the clade‐specific ontogenetic trajectories. It may explain peculiar diversification patterns characteristic to some avian groups, including the long‐leggedness in Ardeidae and tendency for flightlessness in Anatidae.
Book
Morphodynamics is defined as the unique interaction among environment, functional morphology, developmental constraints, phylogeny, and time-all of which shape the evolution of life. These fabricational patterns and similarities owe their regularity not to a detailed genetic program, but to extrinsic factors, which may be mechanical, chemical, or biological in nature. These self-organizing mechanisms are the focus of Morphodynamics. Illustrated by numerous examples from across the biological spectrum, this book embodies the foundation of noted paleontologist Adolf Seilacher’s thinking on the study of morphodynamics. It represents his unique approach of presenting paleontology from an ecological and constructional perspective, rather than a purely taxonomic one. The hallmark of Seilacher’s storied career has been a constructional and functional focus. He begins by discussing the basic principles-form, pattern formation, ecology and evolution, as well as the factors that override those processes. Next, he examines how morphodynamic principles are implemented in various invertebrates including single-celled protists, Ediacarans, sponges, coelenterates, shelled organisms, worms, arthropods, and echinoderms. The final chapter explores how morphogenetic principles may apply to clonal colonial organisms. Summarizing seventy years of research into the interactions of form, function, and evolution, the book is copiously illustrated with the author’s own distinctive drawings and an abundance of photos. It provides a framework for readers to pose their own questions and sharpen their interpretive skills on this fascinating topic.
Article
Parallel evolution across replicate populations has provided evolutionary biologists with iconic examples of adaptation. When multiple populations colonize seemingly similar habitats, they may evolve similar genes, traits, or functions. Yet, replicated evolution in nature or in the laboratory often yields inconsistent outcomes: Some replicate populations evolve along highly similar trajectories, whereas other replicate populations evolve to different extents or in distinct directions. To understand these heterogeneous outcomes, biologists are increasingly treating parallel evolution not as a binary phenomenon but rather as a quantitative continuum ranging from parallel to nonparallel. By measuring replicate populations' positions along this (non)parallel continuum, we can test hypotheses about evolutionary and ecological factors that influence the extent of repeatable evolution. We review evidence regarding the manifestation of (non)parallel evolution in the laboratory, in natural populations, and in applied contexts such as cancer. We enumerate the many genetic, ecological, and evolutionary processes that contribute to variation in the extent of parallel evolution.
Article
Palaeontologists have long employed discrete categorical data to capture morphological variation in fossil species, using the resulting character–taxon matrices to measure evolutionary tempo, infer phylogenies and capture morphological disparity. However, to date these have been seen as separate approaches despite a common goal of understanding morphological evolution over deep time. Here I argue that there are clear advantages to considering these three lines of enquiry in a single space: the phylomorphospace. Conceptually these high‐dimensional spaces capture how a phylogenetic tree explores morphospace and allow us to consider important process questions around evolutionary rates, constraints, convergence and directional trends. Currently the literature contains fundamentally different approaches used to generate such spaces, with no direct comparison between them, despite the differing evolutionary histories they imply. Here I directly compare five different phylomorphospace approaches, three with direct literature equivalents and two that are novel. I use a single empirical case study of coelurosaurian theropod dinosaurs (152 taxa, 853 characters) to show that under many analyses the literature‐derived approaches tend to reflect introduced phylogenetic (rather than the intended morphological) signal. The two novel approaches, which produce limited ancestral state estimates prior to ordination, are able to minimize this phylogenetic signal and thus exhibit more realistic amounts of phylogenetic signal, rate heterogeneity, and convergent evolution.
Article
Taxonomic diversity of benthic marine invertebrate shelf species declines at present by nearly an order of magnitude from the tropics to the poles in each hemisphere along the latitudinal diversity gradient (LDG), most steeply along the western Pacific where shallow-sea diversity is at its tropical maximum. In the Bivalvia, a model system for macroevolution and macroecology, this taxonomic trend is accompanied by a decline in the number of functional groups and an increase in the evenness of taxa distributed among those groups, with maximum functional evenness (FE) in polar waters of both hemispheres. In contrast, analyses of this model system across the two era-defining events of the Phanerozoic, the Permian-Triassic and Cretaceous-Paleogene mass extinctions, show only minor declines in functional richness despite high extinction intensities, resulting in a rise in FE owing to the persistence of functional groups. We hypothesize that the spatial decline of taxonomic diversity and increase in FE along the present-day LDG primarily reflect diversity-dependent factors, whereas retention of almost all functional groups through the two mass extinctions suggests the operation of diversity-independent factors. Comparative analyses of different aspects of biodiversity thus reveal strongly contrasting biological consequences of similarly severe declines in taxonomic diversity and can help predict the consequences for functional diversity among different drivers of past, present, and future biodiversity loss.
Article
Mutation enables evolution, but the idea that adaptation is also shaped by mutational variation is controversial. Simple evolutionary hypotheses predict such a relationship if the supply of mutations constrains evolution, but it is not clear that constraints exist, and, even if they do, they may be overcome by long-term natural selection. Quantification of the relationship between mutation and phenotypic divergence among species will help to resolve these issues. Here we use precise data on over 50,000 Drosophilid fly wings to demonstrate unexpectedly strong positive relationships between variation produced by mutation, standing genetic variation, and the rate of evolution over the last 40 million years. Our results are inconsistent with simple constraint hypotheses because the rate of evolution is very low relative to what both mutational and standing variation could allow. In principle, the constraint hypothesis could be rescued if the vast majority of mutations are so deleterious that they cannot contribute to evolution, but this also requires the implausible assumption that deleterious mutations have the same pattern of effects as potentially advantageous ones. Our evidence for a strong relationship between mutation and divergence in a slowly evolving structure challenges the existing models of mutation in evolution.
Article
The foundations of several disciplines can be expressed as simple quantitative laws, for example, Newton's laws or the laws of thermodynamics. Here I present five laws derived from fossil data that describe the relationships among species extinction and longevity, species richness, origination rates, extinction rates and diversification. These statements of our palaeobiological knowledge constitute a dimension largely hidden from view when studying the living biota, which are nonetheless crucial to the study of evolution and ecology even for groups with poor or non-existent fossil records. These laws encapsulate: the critical fact of extinction; that species are typically geologically short-lived, and thus that the number of extinct species typically dwarfs the number of living species; that extinction and origination rates typically have similar magnitudes; and, that significant extinction makes it difficult to infer much about a clade's early history or its current diversity dynamics from the living biota alone. Although important strides are being made to integrate these core palaeontological findings into our analysis of the living biota, this knowledge needs to be incorporated more widely if we are to understand their evolutionary dynamics.
Article
We compare two major long-term diversifications of marine animal families that began during periods of low diversity but produced strikingly different numbers of phyla, classes, and orders. The first is the early-Paleozoic diversification (late Vendian-Ordovician; 182 MY duration) and the other the Mesozoic phase of the post-Paleozoic diversification (183 MY duration). The earlier diversification was associated with a great burst of morphological invention producing many phyla, classes, and orders and displaying high per taxon rates of family origination. The later diversification lacked novel morphologies recognized as phyla and classes, produced fewer orders, and displayed lower per taxon rates of family appearances. The chief difference between the diversifications appears to be that the earlier one proceeded from relatively narrow portions of adaptive space, whereas the latter proceeded from species widely scattered among adaptive zones and representing a variety of body plans. This difference is believed to explain the major differences in the products of these great radiations. Our data support those models that hold that evolutionary opportunity is a major factor in the outcome of evolutionary processes.
Article
Are measurements of quantitative genetic variation useful for predicting long-term adaptive evolution? To answer this question, I focus on gmax , the multivariate direction of greatest additive genetic variance within populations. Original data on threespine sticklebacks, together with published genetic measurements from other vertebrates, show that morphological differentiation between species has been biased in the direction of gmax for at least four million years, despite evidence that natural selection is the cause of differentiation. This bias toward the direction of evolution tends to decay with time. Rate of morphological divergence between species is inversely proportional to θ, the angle between the direction of divergence and the direction of greatest genetic variation. The direction of greatest phenotypic variance is not identical with gmax , but for these data is nearly as successful at predicting the direction of species divergence. I interpret the findings to mean that genetic variances and covariances constrain adaptive change in quantitative traits for reasonably long spans of time. An alternative hypothesis, however, cannot be ruled out: that morphological differentiation is biased in the direction gmax because divergence and gmax are both shaped by the same natural selection pressures. Either way, the results reveal that adaptive differentiation occurs principally along "genetic lines of least resistance."
Article
Developmental processes represent one of the main constraints on the generation of adult form. Determining how constructional and energetic demands operate throughout growth is es­sential to understanding fundamental growth rules and trade-offs that define the framework within which new species originate. In organisms producing spiral shells, coiling patterns can inform on the constructional constraints acting throughout development that dictated the diversification of forms within a group. Here, we use Synchrotron radiation X-Ray tomographic microscopy (SRXTM) reconstructions of eight planktic foraminifera repre­sentative of the major morphotypic groups to determine disparity of coiling patterns by measuring Raupian parameters. The results show that foraminifera are a morphologically highly conservative group, exploiting a limited range of poten­tial coiling patterns. Very similar coiling patterns during early ontogeny, regardless of species, point toward strong constraints in early ontogeny and to common develop­mental processes acting across all morphogroups. Dispersion and lateral displacement of taxa in morphospace are limited to the adult stage. Accretion with low translation down the coiling axis in juveniles may maximize lateral growth and metabolic efficiency in light of costly calcification. Increased translation in the adult stages allows growth to accommo­date new chamber shapes, mediated by changes in aperture location and the site of accretion over ontogeny. These constructional constraints, and the accretion of a small number of discrete chambers, limit the potential for novel forms within the foraminifera compared to other groups of coiling organisms and may explain the repeated evolution of similar morphotypes throughout the evolutionary history of the group.
Article
Evidence of phenotypic parallelism is often used to infer the deterministic role played by natural selection. However, variation in the extent or direction of divergence is often evident among independent evolutionary replicates, raising the following question: just how parallel, overall, is parallel evolution? We answer this question through a comparative analysis of studies of fishes, a taxon where parallel evolution has been much discussed. We first ask how much of the among-population variance in phenotypic traits can be explained by different “environment” types, such as high predation versus low predation or benthic versus limnetic. We then use phenotypic change vector analysis to quantify variation in the direction (vector angles) and magnitude (vector lengths) of environment-associated divergence. All analyses show high variation in the extent of parallelism—from very high to very low, along with everything in between—highlighting the importance of quantifying parallelism rather than just ...
Article
The influence of within-species variation and covariation on evolutionary patterns is well established for generational and mac- roevolutionary processes, most prominently through genetic lines of least resistance. However, it is not known whether intraspecific pheno- typic variation also directs microevolutionary trajectories into the long term when a species is subject to varying environmental conditions. Here we present a continuous, high-resolution bivariate record of size and shape changes among 12,633 individual planktonic foraminifera of a surviving and an extinct-going species over 500,000 years. Our study interval spans the late Pliocene to earliest Pleistocene intensifi- cation of northern hemisphere glaciation, an interval of profound climate upheaval that can be divided into three phases of increasing glacial in- tensity. Within each of these three Plio-Pleistocene climate phases, the within-population allometries predict evolutionary change from one time step to the next and that the within-phase among-population (i.e., evolutionary) allometries match their corresponding static (within- population) allometries. However, the evolutionary allometry across the three climate phases deviates significantly from the static and phase-specific evolutionary allometries in the extinct-going species. Although intraspecific variation leaves a clear signature on mean evo- lutionary change from one time step to the next, our study suggests that the link between intraspecific variation and longer-term micro- and macroevolutionary phenomena is prone to environmental pertur- bation that can overcome constraints induced by within-species trait covariation.