Reframing research on evolutionary novelty and co-option: Character identity mechanisms versus deep homology

DiFrisco, James; Wagner, Günter P.; Love, Alan C.

doi:10.1016/j.semcdb.2022.03.030

Cited by 30 publications

(24 citation statements)

References 75 publications

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“…We think the time is ripe to undertake new theoretical articulation in relation to serial homology, and in a way that complements and augments recent work of this kind for evolutionary novelty and co‐option (DiFrisco, Wagner & Love, 2022). Here, we adopt a specific tactic to pursue this strategy that involves examining the successful patterns of reasoning that have coalesced in talking about homology at the level of gene sequences (orthology, paralogy, gene families).…”

Section: The Need For Theoretical Articulationmentioning

confidence: 99%

“…It is possible that helmets are serially homologous to wings because they belong to an exite‐derived character family, or the character family of some other basal character, without helmets being wings . Indeed, this seems to be the case (DiFrisco, Wagner & Love, 2022; Fisher et al, 2021). Thus, despite the name “wing serial homologs,” which is commonly used to describe research in this area, wings are evidently too derived to serve as the most evolutionarily informative character for defining the character tree of pleural and tergal outgrowths.…”

Section: Insect Wing Serial Homologsmentioning

confidence: 99%

“…The broad distribution of this regulatory module among diverse body parts suggests it is a generic appendage outgrowth module rather than a ChIM. As we have argued elsewhere (DiFrisco, Wagner & Love, 2022), mechanistic similarity in the development of different body parts can occur for several reasons. The similarity could be due to (i) “plesiomorphic” features that existed in body regions where the new structures are formed, (ii) co‐option, or (iii) a transfer of character identity (e.g., duplication, or homeotic transformation).…”

Section: Paired Gnathostome Appendage Serial Homologymentioning

confidence: 99%

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The hierarchical basis of serial homology and evolutionary novelty

DiFrisco

Love

Wagner

2022

Journal of Morphology

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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 homologs and vertebrate paired appendages.

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Section: The Need For Theoretical Articulationmentioning

confidence: 99%

Section: Insect Wing Serial Homologsmentioning

confidence: 99%

Section: Paired Gnathostome Appendage Serial Homologymentioning

confidence: 99%

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The hierarchical basis of serial homology and evolutionary novelty

DiFrisco

Love

Wagner

2022

Journal of Morphology

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“…Although genes expressed in wings are also expressed in the pronotum, a more nuanced interpretation of the significance of this association is required [ 55 , 56 ]. We suggest that two things must be considered when investigating questions related to treehopper pronotal development and evolution: (i) the genes frequently studied in wings, such as wingless, distal-less, engrailed, hedgehog, spalt, decapentaplegic, apterous, vestigial , are also expressed in, and responsible for the patterning of, other appendages including legs, antennae, mouthparts and genitalia, and also play critical roles earlier, in embryonic development [ 2 , 21 , 57 , 58 ]; and (ii) our observations show that many general features of the adult pronotum are already evident in the 4th instar ( figure 3 ), which suggests that critical transcriptional patterning of pronotal differentiation occurs before the 5th instar.…”

Section: Discussionmentioning

confidence: 99%

The roles of growth regulation and appendage patterning genes in the morphogenesis of treehopper pronota

2022

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Treehoppers of the insect family Membracidae have evolved enlarged and elaborate pronotal structures, which is hypothesized to involve co-opted expression of genes that are shared with the wings. Here, we investigate the similarity between the pronotum and wings in relation to growth. Our study reveals that the ontogenetic allometry of the pronotum is similar to that of wings in Membracidae, but not the outgroup. Using transcriptomics, we identify genes related to translation and protein synthesis, which are mutually upregulated. These genes are implicated in the eIF2, eIF4/p70S6K and mTOR pathways, and have known roles in regulating cell growth and proliferation. We find that species-specific differential growth patterning of the pronotum begins as early as the third instar, which suggests that expression of appendage patterning genes occurs long before the metamorphic molt. We propose that a network related to growth and size determination is the more likely mechanism shared with wings. However, regulators upstream of the shared genes in pronotum and wings need to be elucidated to substantiate whether co-option has occurred. Finally, we believe it will be helpful to distinguish the mechanisms leading to pronotal size from those regulating pronotal shape as we make sense of this spectacular evolutionary innovation.

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“…The prevalence of single or multiple origin(s) of complex traits across the Tree of Life is currently debated 31 . These debates often center on mechanisms that underlie character identity 32 and quality of sampling. Both are relevant here, and our results suggesting multiple gains of RNS do not necessarily conflict with recent findings that critical functional genes, present in at least some NFC outgroups but without nodulation function, were recruited to form a genetic ensemble only once in the ancestor of the NFC 33 .…”

mentioning

confidence: 99%

Two shifts in evolutionary lability underlie independent gains and losses of root-nodule symbiosis in a single clade of plants

Kates

O’Meara

LaFrance

et al. 2022

Preprint

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Root nodule symbiosis (RNS) allows plants to access atmospheric nitrogen converted into usable forms through a mutualistic relationship with soil bacteria. RNS is a complex trait requiring coordination from both the plant host and the bacterial symbiont, and pinpointing the evolutionary origins of root nodules is critical for understanding the genetic basis of RNS. This endeavor is complicated by data limitations and the intermittent presence of RNS in a single clade of ca. 30,000 species of flowering plants, i.e., the nitrogen-fixing clade (NFC). We developed the most extensive de novo phylogeny for all major lineages of the NFC and an enhanced root nodule trait database to reconstruct the evolution of RNS. Through identification of the evolutionary pathway to RNS gain, we show that shifts among heterogeneous evolutionary rates can explain how a complex trait such as RNS can arise many times across a large phylogeny. Our analysis identifies a two-step process in which an ancestral precursor state gave rise to a more labile state from which RNS was quickly gained at specific points in the NFC. Our rigorous reconstruction of ancestral states illustrates how a two-step pathway could have led to multiple independent gains and losses of RNS, contrary to recent hypotheses invoking just a single gain and numerous losses. RNS may be an example of multi-level convergent evolution, thus requiring a broader phylogenetic and genetic scope for genome-phenome mapping to elucidate mechanisms enabling fully functional RNS.

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Reframing research on evolutionary novelty and co-option: Character identity mechanisms versus deep homology

Cited by 30 publications

References 75 publications

The hierarchical basis of serial homology and evolutionary novelty

The hierarchical basis of serial homology and evolutionary novelty

The roles of growth regulation and appendage patterning genes in the morphogenesis of treehopper pronota

Two shifts in evolutionary lability underlie independent gains and losses of root-nodule symbiosis in a single clade of plants

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