Fig 2 - uploaded by James DiFrisco
Content may be subject to copyright.
Selectional DSD. A pleiotropic gene (or gene complex) controls characters A and B. B starts to undergo directional selection in the right-side lineage, causing gene2 to replace gene1, while stabilizing selection on A favours compensatory genetic changes that maintain the A phenotype. The result is that character A remains homologous across the pictured monophyletic group despite having different genetic causes in the different lineages.
Source publication
Advances in developmental genetics and evo-devo in the last several decades have enabled the growth of novel developmental approaches to the classic theme of homology. These approaches depart from the more standard phylogenetic view by contending that homology between morphological characters depends on developmental-genetic individuation and expla...
Citations
... contention about homology and levels-namely, that homology between characters at one level is often independent of homology at another level. While acknowledging this fact, the central hypothesis of the ChIM model is that character identity is linked to the identity of specific underlying (i.e., lower-level) mechanisms, which are subsets of the total developmental mechanism for building a body part in a particular species (DiFrisco, 2021). ...
Given the pervasiveness of gene sharing in evolution and the extent of homology across the tree of life, why is everything not homologous with everything else? The continuity and overlapping genetic contributions to diverse traits across lineages seem to imply that no discrete determination of homology is possible. Although some argue that the widespread overlap in parts and processes should be acknowledged as "partial" homology, this threatens a broad base of presumed comparative morphological knowledge accepted by most biologists. Following a long scientific tradition, we advocate a strategy of "theoretical articulation" that introduces further distinctions to existing concepts to produce increased contrastive resolution among the labels used to represent biological phenomena. We pursue this strategy by drawing on successful patterns of reasoning from serial homology at the level of gene sequences to generate an enriched characterization of serial homology as a hierarchical, phylogenetic concept. Specifically, we propose that the concept of serial homology should be applied primarily to repeated but developmentally individualized body parts, such as cell types, differentiated body segments, or epidermal appendages. For these characters, a phylogenetic history can be reconstructed, similar to families of paralogous genes, endowing the notion of serial homology with a hierarchical, phylogenetic interpretation. On this basis, we propose a five-fold theoretical classification that permits a more fine-grained mapping of diverse trait-types. This facilitates answering the question of why everything is not homologous with everything else, as well as how novelty is possible given that any new character possesses evolutionary precursors. We illustrate the fecundity of our account by reference to debates over insect wing serial homologues and vertebrate paired appendages. This article is protected by copyright. All rights reserved.
... Canonically, reconstructions of morphogenetic evolution have been hypothesized by extrapolating that (apparently) homologous states develop in the same manner among extinct and extant taxa (for this study, mediad overhang of the femoral head). However, morphogenesis can change while adult phenotypes remain static [61][62][63][64][65][66][67][68]. Potentially, the same developmental processes among different species can be misinterpreted as disparate, especially when they occur in different situations (e.g. ...
Significant evolutionary shifts in locomotor behaviour often involve comparatively subtle anatomical transitions. For dinosaurian and avian evolution, medial overhang of the proximal femur has been central to discussions. However, there is an apparent conflict with regard to the evolutionary origin of the dinosaurian femoral head, with neontological and palaeontological data suggesting seemingly incongruent hypotheses. To reconcile this, we reconstructed the evolutionary history of morphogenesis of the proximal end of the femur from early archosaurs to crown birds. Embryological comparison of living archosaurs (crocodylians and birds) suggests the acquisition of the greater overhang of the femoral head in dinosaurs results from additional growth of the proximal end in the medial-ward direction. On the other hand, the fossil record suggests that this overhang was acquired by torsion of the proximal end, which projected in a more rostral direction ancestrally. We reconcile this apparent conflict by inferring that the medial overhang of the dinosaur femoral head was initially acquired by torsion, which was then superseded by mediad growth. Details of anatomical shifts in fossil forms support this hypothesis, and their biomechanical implications are congruent with the general consensus regarding broader morpho-functional evolution on the avian stem.
... Without a conceptual framework with empirical predictions for what underwrites character identity, or a character identity mechanism [11], it is difficult to operationalize what it would mean for a new character identity to originate and how we would go about testing ideas about character origination. This is especially pertinent given that homologous characters can develop from different and often diverse sets of developmental processes [12][13][14]. Second, many attempts to explain the evolutionary origins of novelty depend on appeals to the phenomenon of co-option. ...
... These mechanisms include not just genes or other components but also their dynamics and the organization of parts and activities that generate phenotypic outcomes. Importantly, these additional aspects of mechanism facilitate tracing the evolutionary continuity of a mechanism through changes in its participating genes-a process known as "developmental system drift" [12][13][14]. ChIMs not only undergird the evolutionary continuity of morphological characters, enabling them to stand in phylogenetic relations of homology, but they are themselves homologues with evolutionary coherence and repeatability across generations and species [11]. ...
A central topic in research at the intersection of development and evolution is the origin of novel traits. Despite progress on understanding how developmental mechanisms underlie patterns of diversity in the history of life, the problem of novelty continues to challenge researchers. Here we argue that research on evolutionary novelty and the closely associated phenomenon of co-option can be reframed fruitfully by: (1) specifying a conceptual model of mechanisms that underwrite character identity, (2) providing a richer and more empirically precise notion of co-option that goes beyond common appeals to “deep homology”, and (3) attending to the nature of experimental interventions that can determine whether and how the co-option of identity mechanisms can help to explain novel character origins. This reframing has the potential to channel future investigation to make substantive progress on the problem of evolutionary novelty. To illustrate this potential, we apply our reframing to two case studies: treehopper helmets and beetle horns.
... This is not to say that this approach and the ChIM model on which it relies are free from limitations. Most notably, in their current form they do not make any strong attempt to incorporate relevant extrinsic factors such as ecological pressures and certain intrinsic factors such as physico-chemical constraints on characters in the study of homology, and the ChIM model has difficulty capturing morphological traits which don't obviously have a ChIM and are rather "by-products" of other ChIMs, such as the human chin (DiFrisco, 2020;DiFrisco et al., 2020). Nonetheless, the ChIM model has notable merits besides those discussed above, including retaining the explanatory strengths of the ChIN model and extending its breadth of scope, as well as providing more than one "handle for homology"-which means their homology (not homology of the characters they underlie) can be assessed by several means, which allows for utilising different such means in different situations. ...
... This is not to say that this approach and the ChIM model on which it relies are free from limitations. Most notably, in their current form they do not make any strong attempt to incorporate relevant extrinsic factors such as ecological pressures and certain intrinsic factors such as physico-chemical constraints on characters in the study of homology, and the ChIM model has difficulty capturing morphological traits which don't obviously have a ChIM and are rather "by-products" of other ChIMs, such as the human chin (DiFrisco, 2020;DiFrisco et al., 2020). Nonetheless, the ChIM model has notable merits besides those discussed above, including retaining the explanatory strengths of the ChIN model and extending its breadth of scope, as well as providing more than one "handle for homology"-which means their homology (not homology of the characters they underlie) can be assessed by several means, which allows for utilising different such means in different situations. ...
This thesis is about the complicated and multifaceted problem of the evolution of the
eumetazoan body plan and its key role in the emergence of organismal complexity in
the animal kingdom. As such, it draws on a very broad range of topics and discussions
including empirical research programmes in palaeontology, comparative morphology,
classical and genetic developmental biology, and morphological and molecular
phylogenetics; as well as theoretical/philosophical research around the conceptual
bases of phylogenetics, homology, scientific integration, and biological complexity and
individuality. In the following chapters, I first provide background on and an outline
of the thesis (chapter 1); I then propose an overarching conceptual framework for the
integration of different kinds of evidence in macroevolutionary biology (chapter 2),
with a special emphasis on the integration of morphological and developmental genetic
evidence in inferring morphological homology (chapter 3); followed by providing a
phylogeny of the major animal groups incorporating the two Ediacaran fossils
Dickinsonia and Yorgia (chapter 4) and building on this phylogenetic placement to
propose a novel evolutionary scenario for the evolution of key features of the
eumetazoan body plan—namely the gastric cavity and bilateral symmetry—in light of
Dickinsonia and other Ediacaran fossils (chapter 5). I finish with a discussion on the
evolution of complexity in the animal kingdom in light of preceding chapters and the
multilevel selection literature (chapter 6), and a brief final conclusion.
... This is not to say that this approach and the ChIM model on which it relies are free from limitations. Most notably, in their current form they do not make any strong attempt to incorporate relevant extrinsic factors such as ecological pressures and certain intrinsic factors such as physico-chemical constraints on characters in the study of homology, and the ChIM her ChIMs, such as the human chin (DiFrisco, 2020;DiFrisco et al., 2020). Nonetheless, the ChIM model has notable merits besides those discussed above, including retaining the explanatory strengths of the ChIN model and extending its breadth of which means their homology (not homology of the characters they underlie) can be assessed by several means, which allows for utilising different such means in different situations. ...
... This is not to say that this approach and the ChIM model on which it relies are free from limitations. Most notably, in their current form they do not make any strong attempt to incorporate relevant extrinsic factors such as ecological pressures and certain intrinsic factors such as physico-chemical constraints on characters in the study of homology, and the ChIM her ChIMs, such as the human chin (DiFrisco, 2020;DiFrisco et al., 2020). Nonetheless, the ChIM model has notable merits besides those discussed above, including retaining the explanatory strengths of the ChIN model and extending its breadth of which means their homology (not homology of the characters they underlie) can be assessed by several means, which allows for utilising different such means in different situations. ...
Reconstructing ancestral species is a challenging endeavour: fossils are often scarce or enigmatic, and inferring ancestral characters based on novel molecular approaches (e.g. comparative genomics or developmental genetics) has long been controversial. A key philosophical challenge pertinent at present is the lack of a theoretical framework capable of evaluating inferences of homology made through integration of multiple kinds of evidence (e.g. molecular, developmental, or morphological). Here, I present just such a framework. I start with a brief history and critical assessment of attempts at inferring morphological homology through developmental genetics. I then bring attention to a recent model of homology, namely Character Identity Mechanisms (DiFrisco, Love, & Wagner, 2020), intended partly to elucidate the relationships between morphological characters, developmental genetics, and homology. I utilise and build on this model to construct the evaluative framework mentioned above, which judges the epistemic value of evidence of each kind in each particular case based on three proposed criteria: effectiveness, admissibility, and informativity, as well as providing a generalised guideline on how it can be scientifically operationalised. I then point out the evolution of the eumetazoan body plan as a case in point where the application of this framework can yield satisfactory results, both empirically and conceptually. I will conclude with a discussion on some potential implications for more general philosophy of biology and philosophy of science, especially surrounding evidential integration, models and explanation, and reductionism.
... This is the approach we take to the demarcation of processes here-namely, to allow the applicability of the proposed criteria of process homology to distinguish the processes that are well-defined enough to be homologized from those that are not. A more general ontology of biological processes would, like a theory of characters, be a helpful addition to this project but is not a necessary precondition for it (for some existing resources, see Dupré 2017; Nicholson and Dupré 2018;Seibt 2020;DiFrisco 2021). ...
Comparative biology builds up systematic knowledge of the diversity of life, across evolutionary lineages and levels of organization, starting with evidence from a sparse sample of model organisms. In developmental biology, a key obstacle to the growth of comparative approaches is that the concept of homology is not very well defined for levels of organization that are intermediate between individual genes and morphological characters. In this paper, we investigate what it means for ontogenetic processes to be homologous, focusing specifically on the examples of insect segmentation and vertebrate somitogenesis. These processes can be homologous without homology of the underlying genes or gene networks, since the latter can diverge over evolutionary time, while the dynamics of the process remain the same. Ontogenetic processes like these therefore constitute a dissociable level and distinctive unit of comparison requiring their own specific criteria of homology. In addition, such processes are typically complex and nonlinear, such that their rigorous description and comparison not only requires observation and experimentation, but also dynamical modeling. We propose six criteria of process homology, combining recognized indicators (sameness of parts, morphological outcome, and topological position) with novel ones derived from dynamical systems modeling (sameness of dynamical properties, dynamical complexity, and evidence for transitional forms). We show how these criteria apply to animal segmentation and other ontogenetic processes. We conclude by situating our proposed dynamical framework for homology of process in relation to similar research programs, such as process structuralism and developmental approaches to morphological homology.
The intersection of development and evolution has always harbored conceptual issues, but many of these are on display in contemporary evolutionary developmental biology (evo-devo). These issues include: (1) the precise constitution of evo-devo, with its focus on both the evolution of development and the developmental basis of evolution, and how it fits within evolutionary theory; (2) the nature of evo-devo model systems that comprise the material of comparative and experimental research; (3) the puzzle of how to understand the widely used notion of 'conserved mechanisms'; (4) the definition of evolutionary novelties and expectations for how to explain them; and (5) the demand of interdisciplinary collaboration that derives from investigating complex phenomena at key moments in the history of life, such as the fin-limb transition. This Element treats these conceptual issues with close attention to both empirical detail and scientific practice to offer new perspectives on evolution and development. This title is also available as Open Access on Cambridge Core.
The discovery of general principles underlying the complexity and diversity of cellular and developmental systems is a central and long-standing aim of biology. Whilst new technologies collect data at an ever-accelerating rate, there is growing concern that conceptual progress is not keeping pace. We contend that this is due to a paucity of appropriate conceptual frameworks to serve as a basis for general theories of mesoscale biological phenomena. In exploring this issue, we have developed a foundation for one such framework, termed the Core and Periphery (C&P) hypothesis, which reveals hidden generality across the diverse and complex behaviors exhibited by cells and tissues. Here, we present the C&P concept, provide examples of its applicability across multiple scales, argue its consistency with evolution, and discuss key implications and open questions. We propose that the C&P hypothesis could unlock new avenues of conceptual progress in cell and developmental biology.
The term "homology" is persistently polysemous, defying the expectation that extensive scientific research should yield semantic stability. A common response has been to seek a unification of various prominent definitions. This paper proposes an alternative strategy, based on the insight that scientific concepts function as tools for research: When analyzing various conceptualizations of homology, we should preserve those distinguishing features that support particular research goals. We illustrate the fruitfulness of our strategy by application to two cases. First, we revisit Lankester's celebrated evolutionary reappraisal of homology and argue that his analysis has been distorted by assimilation to modern agendas. His "homogeny" does not mean the same thing as modern evolutionary "homology," and his "homoplasy" is no mere antonym. Instead, Lankester uses both new terms to pose a question that remains strikingly relevant-how do mechanistic and historical causes of morphological resemblance interact? Second, we examine the puzzle of avian digit homology, which exemplifies disciplinary differences in homology conceptualization and assessment. Recent progress has been fueled by the development of new tools within the relevant disciplines (paleontology and developmental biology) and especially by increasing interdisciplinary cooperation. Conceptual unification has played very little role in this work, which instead seeks concrete evolutionary scenarios that integrate all the available evidence. Together these cases indicate the complex relationship between concepts and other tools in homology research.
The origin of RNA interference (RNAi) is usually explained by a defense-based hypothesis, in which RNAi evolved as a defense against transposable elements (TEs) and RNA viruses and was already present in the last eukaryotic common ancestor (LECA). However, since RNA antisense regulation and double-stranded RNAs (dsRNAs) are ancient and widespread phenomena, the origin of defensive RNAi should have occurred in parallel with its regulative functions to avoid imbalances in gene regulation. Thus, we propose a neutral evolutionary hypothesis for the origin of RNAi in which qualitative system drift from a prokaryotic antisense RNA (asRNA) gene regulation mechanism leads to the formation of RNAi through constructive neutral evolution (CNE). We argue that RNAi was already present in the ancestor of LECA before the need for a new defense system arose and that its presence helped to shape eukaryotic genomic architecture and stability.
