Plasticity‐led evolution: A survey of developmental mechanisms and empirical tests

Recent years have witnessed increased interest in evaluating whether phenotypic plasticity can precede, facilitate, and possibly even bias adaptive evolution. Despite accumulating evidence for “plasticity‐led evolution” (i.e., “PLE”), critical gaps remain, such as: how different developmental mechanisms influence PLE; whether some types of traits and taxa are especially prone to experience PLE; and what studies are needed to drive the field forward. Here, we begin to address these shortcomings by first speculating about how various features of development—modularity, flexible regulation, and exploratory mechanisms—might impact and/or bias whether and how PLE unfolds. We then review and categorize the traits and taxa used to investigate PLE. We do so both to identify systems that may be well‐suited for studying developmental mechanisms in a PLE context and to highlight any mismatches between PLE theory and existing empirical tests of this theory. We conclude by providing additional suggestions for future research. Our overarching goal is to stimulate additional work on PLE and thereby evaluate plasticity's role in evolution.     

Developmental bias,macroevolution, and the fossil record

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.     

Animal learning as a source of developmental bias

As a form of adaptive plasticity that allows organisms to shift their phenotype toward the optimum, learning is inherently a source of developmental bias. Learning may be of particular significance to the evolutionary biology community because it allows animals to generate adaptively biased novel behavior tuned to the environment and, through social learning, to propagate behavioral traits to other individuals, also in an adaptively biased manner. We describe several types of developmental bias manifest in learning, including an adaptive bias, historical bias, origination bias, and transmission bias, stressing that these can influence evolutionary dynamics through generating nonrandom phenotypic variation and/or nonrandom environmental states. Theoretical models and empirical data have established that learning can impose direction on adaptive evolution, affect evolutionary rates (both speeding up and slowing down responses to selection under different conditions) and outcomes, influence the probability of populations reaching global optimum, and affect evolvability. Learning is characterized by highly specific, path‐dependent interactions with the (social and physical) environment, often resulting in new phenotypic outcomes. Consequently, learning regularly introduces novelty into phenotype space. These considerations imply that learning may commonly generate plasticity first evolution.     

Taxonomic identification bias does not drive patterns of abundance and diversity in theropod dinosaurs

The ability of palaeontologists to correctly diagnose and classify new fossil species from incomplete morphological data is fundamental to our understanding of evolution. Different parts of the vertebrate skeleton have different likelihoods of fossil preservation and varying amounts of taxonomic information, which could bias our interpretations of fossil material. Substantial previous research has focused on the diversity and macroevolution of non-avian theropod dinosaurs. Theropods provide a rich dataset for analysis of the interactions between taxonomic diagnosability and fossil preservation. We use specimen data and formal taxonomic diagnoses to create a new metric, the Likelihood of Diagnosis, which quantifies the diagnostic likelihood of fossil species in relation to bone preservation potential. We use this to assess whether a taxonomic identification bias impacts the non-avian theropod fossil record. We find that the patterns of differential species abundance and clade diversity are not a consequence of their relative diagnosability. Although there are other factors that bias the theropod fossil record that are not investigated here, our results suggest that patterns of relative abundance and diversity for theropods might be more representative of Mesozoic ecology than often considered.     

Conceptual and analytical worldviews shape differences about global avian biogeography

In a recent paper, we generated a new time tree of modern birds and integrated it with biogeographic and palaeontological information to formulate a model for their biogeographic history. We postulated that modern birds originated in West Gondwanan continents, from where they dispersed around the world. Mayr suggested that our selective use of the fossil record may have biased our ancestral area reconstructions. We argue that the use of the fossil record must be selective in order to avoid the influence of its severe geographic bias: rock formations with numerous high‐quality fossil birds are found only in North America and Europe. An indiscriminate use of the avian fossil record would bias any biogeographic analysis towards these two continents. Our biogeographic model is perfectly consistent with the existence of diverse fossil avifaunas in the Eocene of North America and Europe because dispersion out of South America occurred earlier, in the Palaeocene.     

Evolution and development of the mammalian jaw joint: Making a novel structure

A jaw joint between the squamosal and dentary is a defining feature of mammals and is referred to as the temporomandibular joint (TMJ) in humans. Driven by changes in dentition and jaw musculature, this new joint evolved early in the mammalian ancestral lineage and permitted the transference of the ancestral jaw joint into the middle ear. The fossil record demonstrates the steps in the cynodont lineage that led to the acquisition of the TMJ, including the expansion of the dentary bone, formation of the coronoid process, and initial contact between the dentary and squamosal. From a developmental perspective, the components of the TMJ form through tissue interactions of muscle and skeletal elements, as well as through interaction between the jaw and the cranial base, with the signals involved in these interactions being both biomechanical and biochemical. In this review, we discuss the development of the TMJ in an evolutionary context. We describe the evolution of the TMJ in the fossil record and the development of the TMJ in embryonic development. We address the formation of key elements of the TMJ and how knowledge from developmental biology can inform our understanding of TMJ evolution.     

Palaeontology and Evolutionary Developmental Biology: A Science of the Nineteenth and Twenty–first Centuries

A wind of change has swept through palaeontology in the past few decades. Contrast Sir Peter Medawar’s dismissive: ‘palaeontology is a particularly undemanding branch of science’ (as recalled by John Maynard Smith in Sabbagh 1999, p. 158) with ‘Palaeontology: grasping the opportunities in the science of the twenty–first century’, the title of a contribution to a special issue of Geobios by the Cambridge palaeontologist, Simon Conway Morris (1998a). The winds of change have come partly from palaeontologists seeking to broaden the impact of their studies and partly from biologists (neontologists) realizing the contributions that palaeontology can make to their disciplines. Consequently, impressions of past life preserved in stone are coming alive. Fossils are being described and analyzed using new tools and languages as the static fossil record becomes a record of transitions in patterns that can be explained and related to biological, ecological, climatic and tectonic changes. The latest addition is evolutionary developmental biology, or ‘evo–devo’, whose language provides a new basis upon which to interpret anatomical change, both materially and mechanistically. In this review I examine the major contributions made by palaeontology, how palaeontology has been linked to evolution and to embryology in the past, and how links with evo–devo have enlivened and will continue to enliven both palaeontology and evo–devo. Closer links between the two fields should illuminate important unresolved issues related to the origin of the metazoans (e.g. Why is there a conflict between molecular clocks and the fossil record in timing the metazoan radiation; were Precambrian metazoan ancestors similar to extant larvae or to miniature adults?) and to diversification of the metazoans (e.g. How do developmental constraints bias the direction of evolution; how do microevolutionary developmental processes relate to macroevolutionary changes?).     

Fossilized embryos are widespread but the record is temporally and taxonomically biased

We report new discoveries of embryos and egg capsules from the Lower Cambrian of Siberia, Middle Cambrian of Australia and Lower Ordovician of North America. Together with existing records, embryos have now been recorded from four of the seven continents. However, the new discoveries highlight secular and systematic biases in the fossil record of embryonic stages. The temporal window within which the embryos and egg capsules are found is of relatively short duration; it ends in the Early Ordovician and is roughly coincident with that of typical "Orsten"-type faunas. The reduced occurrence of such fossils has been attributed to reducing levels of phosphate in marine waters during the early Paleozoic, but may also be owing to the increasing depth of sediment mixing by infaunal metazoans. Furthermore, most records younger than the earliest Cambrian are of a single kind-large eggs and embryos of the priapulid-like scalidophoran Markuelia. We explore alternative explanations for the low taxonomic diversity of embryos recovered thus far, including sampling, size, anatomy, ecology, and environment, concluding that the preponderance of Markuelia embryos is due to its precocious development of cuticle at an embryonic stage, predisposing it to preservation through action as a substrate on which microbially mediated precipitation of authigenic calcium phosphate may occur. The fossil record of embryos may be limited to a late Neoproterozoic to early Ordovician snapshot that is subject to dramatic systematic bias. Together, these biases must be considered seriously in attempts to use the fossil record to arbitrate between hypotheses of developmental and life history evolution implicated in the origin of metazoan clades.     

埃迪卡拉纪至寒武纪苗岭世刺细胞动物化石研究现状与展望

刺细胞动物是一类具有刺细胞的水生无脊椎动物,分布在世界各地的海洋和淡水中.作为后生动物最早分化出的一支,刺细胞动物对研究后生动物的起源和早期演化具有极其重要的意义,也为研究后生动物系统发育、地层对比和古地理恢复等方面提供了重要的科研线索.本文简要介绍了刺细胞动物早期(埃迪卡拉纪至寒武纪苗岭世)的化石记录和研究现状,将刺...     

Developmental noise and ecological opportunity across space can release constraints on the evolution of plasticity

Phenotypic plasticity is a potentially definitive solution to environment heterogeneity, driving biologists to understand why it is not ubiquitous in nature. While costs and constraints may limit the success of plasticity, we are still far from a complete theory of when these limitations actually proscribe adaptive plasticity. Here I use a simple model of plasticity incorporating developmental noise to explore the competitive and evolutionary relationships of specialist and generalist genotypes spreading across a heterogeneous landscape. Results show that plasticity can arise in the context of specialism, preadapting genotypes to later evolve toward plastic generalism. Developmental noise helps a mutant with imperfect plasticity successfully compete against its ancestor, providing an evolutionary path by which subsequent mutations can refine plasticity toward its optimum. These results address how the complex selection pressures across a heterogeneous environment can help evolution find paths around constraints arising from developmental mechanisms.     

Developmental plasticity and evolution—quo vadis?

The role of developmental (phenotypic) plasticity in ecology and evolution is receiving a growing appreciation among the biologists, and many plasticity-specific concepts have become well established as part of the mainstream evolutionary biological thinking. In this essay, I posit that despite this progress several key perspectives in developmental plasticity remain remarkably traditional, and that it may be time to re-evaluate their continued usefulness in the face of the available evidence as the field looks to its future. Specifically, I discuss the utility of viewing plastic development as ultimately rooted in genes and genomes, and investigate the common notion that the environment—albeit a critical source of information—nevertheless remains passive, external to and separable from the organism responding to it. I end by highlighting conceptual and empirical opportunities that may permit developmental plasticity research to transcend its current boundaries and to continue its contributions toward a holistic and realistic understanding of organismal development and evolution.     

Towards “A Natural History of Data”: Evolving Practices and Epistemologies of Data in Paleontology, 1800–2000

The fossil record is paleontology’s great resource, telling us virtually everything we know about the past history of life. This record, which has been accumulating since the beginning of paleontology as a professional discipline in the early nineteenth century, is a collection of objects. The fossil record exists literally, in the specimen drawers where fossils are kept, and figuratively, in the illustrations and records of fossils compiled in paleontological atlases and compendia. However, as has become increasingly clear since the later twentieth century, the fossil record is also a record of data. Paleontologists now routinely abstract information from the physical fossil record to construct databases that serve as the basis for quantitative analysis of patterns in the history of life. What is the significance of this distinction? While it is often assumed that the orientation towards treating the fossil record as a record of data is an innovation of the computer age, it turns out that nineteenth century paleontology was substantially “data driven.” This paper traces the evolution of data practices and analyses in paleontology, primarily through examination of the compendia in which the fossil record has been recorded over the past 200 years. I argue that the transition towards conceptualizing the fossil record as a record of data began long before the emergence of the technologies associated with modern databases (such as digital computers and modern statistical methods). I will also argue that this history reveals how new forms of visual representation were associated with the transition from seeing the fossil record as a record of objects to one of data or information, which allowed paleontologists to make new visual arguments about their data. While these practices and techniques have become increasingly sophisticated in recent decades, I will show that their basic methodology was in place over a century ago, and that, in a sense, paleontology has always been a “data driven” science.     

Developmental plasticity associated with early structural integration and evolutionary patterns: Examples of developmental bias and developmental facilitation in the skeletal system

The relation of developmental plasticity to evolutionary diversification is a key component of evolutionary theory involving developmental bias, but the basis of the relationship varies among traits and among taxa. Here I review some scenarios of how structural integration during early organogenesis could influence this relationship. When condensations are highly integrated and dependent on each other during early organogenesis, both plasticity and evolution are restricted, for example size proportions in molar tooth rows and phalanges within a digit. When similar condensations develop and remain separate (in tracheal cartilages and feather buds), they show high levels of variation and diversity in number but not in shape and size, at least at early stages. When non‐similar structures form separately and then integrate while still undergoing patterning, high levels of plasticity (in number, size, shape; in rib uncinate processes) or new dimensions of ecologically‐significant variation (cusp offset, in mammal teeth) are seen. Although each of these structural integration scenarios is unique, the modulation of evolvability is detectable and informative. Parsing the influence of structural integration at these developmental levels, rather than later‐stage structural correlations or only through genetic covariation, may be necessary to advance understanding of evolvability of the phenotype.     

Does phenotypic plasticity initiate developmental bias?

The generation of variation is paramount for the action of natural selection. Although biologists are now moving beyond the idea that random mutation provides the sole source of variation for adaptive evolution, we still assume that variation occurs randomly. In this review, we discuss an alternative view for how phenotypic plasticity, which has become well accepted as a source of phenotypic variation within evolutionary biology, can generate nonrandom variation. Although phenotypic plasticity is often defined as a property of a genotype, we argue that it needs to be considered more explicitly as a property of developmental systems involving more than the genotype. We provide examples of where plasticity could be initiating developmental bias, either through direct active responses to similar stimuli across populations or as the result of programmed variation within developmental systems. Such biased variation can echo past adaptations that reflect the evolutionary history of a lineage but can also serve to initiate evolution when environments change. Such adaptive programs can remain latent for millions of years and allow development to harbor an array of complex adaptations that can initiate new bouts of evolution. Specifically, we address how ideas such as the flexible stem hypothesis and cryptic genetic variation overlap, how modularity among traits can direct the outcomes of plasticity, and how the structure of developmental signaling pathways is limited to a few outcomes. We highlight key questions throughout and conclude by providing suggestions for future research that can address how plasticity initiates and harbors developmental bias.     

A striking example of developmental bias in an evolutionary process: The “domestication syndrome”

The question of whether “developmental bias” can influence evolution is still controversial, despite much circumstantial evidence and a good theoretical argument. Here, I will argue that the domestication of mammalian species, which took place independently more than two dozen times, provides a particularly convincing example of developmental bias in evolution. The singular finding that underlies this claim is the repeated occurrence in domesticated mammals of a set of distinctive traits, none of which were deliberately selected. This phenomenon has been termed “the domestication syndrome”. In this article, I will: (a) describe the properties of the domestication syndrome; (b) show how it can be explained in terms of the operation of a specific genetic regulatory network, that which governs neural crest cell development; and (c) discuss Dmitry Belyaev's idea of “destabilizing selection,” which holds that selecting for a new behavior often entails neuroendocrine alterations that alter many aspects of development. Finally, I will argue for the potential general significance of such destabilizing selection, in combination with developmental bias, in animal evolution.     

To what extent do new fossil discoveries change our understanding of clade evolution? A cautionary tale from burying beetles (Coleoptera: Nicrophorus)

Divergence time estimates derived from phylogenies are crucial to infer historical biogeography and diversification dynamics. Yet, the impact of fossil record incompleteness on macroevolutionary reconstructions remains equivocal. Here, we investigate to what extent gaps in the fossil record can impinge downstream evolutionary inferences in the beetle family Silphidae. Recent discoveries have pushed back the fossil record of this group from the Eocene into the Jurassic. We estimated the divergence times of the family using both its currently understood fossil record and the fossil record known prior to these recent discoveries. All fossil calibrations were informed with different parametric distributions to investigate the weight of priors on posterior age estimates. Based on time‐calibrated trees, we assessed the impact of fossil calibrations on the inference of ancestral ranges and diversification rate dynamics in the genus Nicrophorus. Depending upon the selected sets of fossil constraints, the age discrepancies had a major impact on the macroevolutionary inferences: the biogeographic extrapolations relative to paleogeography are markedly contrasting, and the calculated rates at which species form or go extinct (and when they varied) are strikingly different. We show that soft prior distributions do not necessarily alleviate such shortcomings therefore preventing the inference of reliable macroevolutionary patterns in groups presenting a taphonomic bias in their fossil record.     

A new species of Kolpochoerus (Mammalia: Suidae) from the Pliocene of Central Afar, Ethiopia: Its Taxonomy and Phylogenetic Relationships

Kolpochoerus (Mammalia: Suidae) is a suine genus represented by a number of species from Plio-Pleistocene sites in Africa. While the general trends in Kolpochoerus evolution are broadly known, gaps in the fossil record preclude an understanding of the details of its evolutionary tempo and mode. Here, we describe a new species, Kolpochoerus millensis, based on new fossil material from the Woranso-Mille and Gona sites in the Central Afar region of Ethiopia and dated to 3.5–3.8 million years ago (Ma). Third molars of K. millensis are metrically and morphologically intermediate between the early Pliocene K. deheinzelini and earliest late Pliocene K. afarensis. It appears that K. deheinzelini, K. millensis, and K. afarensis are temporally disjunct and phenetically distinguishable parts of a single evolving lineage. The recognition of these chronospecies provides additional evidence for anagenetic evolution. It demonstrates clearly the presence of transitional forms in the fossil record. The extensive and well-dated Kolpochoerus fossil record serves as one of the best documented examples of the occurrence of phyletic evolution. Moreover, K. millensis is one of the best biochronological markers in eastern Africa for the time between 3.5 and 3.8 Ma.     

How much can we know about the causes of evolutionary trends?

One of the first questions that paleontologists ask when they identify a large-scale trend in the fossil record (e.g., size increase, complexity increase) is whether it is passive or driven. In this article, I explore two questions about driven trends: (1) what is the underlying cause or source of the directional bias? and (2) has the strength of the directional bias changed over time? I identify two underdetermination problems that prevent scientists from giving complete answers to these two questions.     

Decay of vertebrate characters in hagfish and lamprey (Cyclostomata) and the implications for the vertebrate fossil record

The timing and sequence of events underlying the origin and early evolution of vertebrates remains poorly understood. The palaeontological evidence should shed light on these issues, but difficulties in interpretation of the non-biomineralized fossil record make this problematic. Here we present an experimental analysis of decay of vertebrate characters based on the extant jawless vertebrates (Lampetra and Myxine). This provides a framework for the interpretation of the anatomy of soft-bodied fossil vertebrates and putative cyclostomes, and a context for reading the fossil record of non-biomineralized vertebrate characters. Decay results in transformation and non-random loss of characters. In both lamprey and hagfish, different types of cartilage decay at different rates, resulting in taphonomic bias towards loss of 'soft' cartilages containing vertebrate-specific Col2α1 extracellular matrix proteins; phylogenetically informative soft-tissue characters decay before more plesiomorphic characters. As such, synapomorphic decay bias, previously recognized in early chordates, is more pervasive, and needs to be taken into account when interpreting the anatomy of any non-biomineralized fossil vertebrate, such as Haikouichthys, Mayomyzon and Hardistiella.     

Evolutionary Development in Australopithecus africanus

Evolutionary developmental biology is quickly transforming our understanding of how lineages evolve through the modification of ontogenetic processes. Yet, while great strides have been made in the study of neontological forms, it is much more difficult to apply the principles of evo-devo to the miserly fossil record. Because fossils are static entities, we as researchers can only infer evolution and development by drawing connections between them. The choices of how we join specimens together??juveniles to adults to study ontogeny, taxon to taxon to study evolution??can dramatically affect our results. Here, I examine paedomorphism in the fossil hominin species Australopithecus africanus. Using extant African apes as proxies for ancestral hominin morphology, I demonstrate that Sts 71 is most similar to a sub-adult African ape, suggesting that A. africanus is paedomorphic relative to the presumed ancestral form. I then plot ontogenetic size and shape in extant great apes, humans, and A. africanus in order to assess patterns of ontogenetic allometry. Results indicate that ontogenetic allometry in A. africanus, subsequent to M1 occlusion is similar to that in modern humans and bonobos; gorillas, chimpanzees, and orangutans share a different pattern of size-shape relationship. Combined with results from the analysis of paedomorphism plus knowledge about the developmental chronologies of this group, these findings suggest that paedomorphism in A. africanus arises relatively early in ontogeny.