Character Identity Networks Research Articles

Pushing the boundaries of organ identity: Homology of the grass lemma

Pushing the boundaries of organ identity: Homology of the grass lemma

Ancestral regulatory mechanisms specify conserved midbrain circuitry in arthropods and vertebrates

Corresponding attributes of neural development and function suggest arthropod and vertebrate brains may have an evolutionarily conserved organization. However, the underlying mechanisms have remained elusive. Here, we identify a gene regulatory and character identity network defining the deutocerebral-tritocerebral boundary (DTB) in Drosophila This network comprises genes homologous to those directing midbrain-hindbrain boundary (MHB) formation in vertebrates and their closest chordate relatives. Genetic tracing reveals that the embryonic DTB gives rise to adult midbrain circuits that in flies control auditory and vestibular information processing and motor coordination, as do MHB-derived circuits in vertebrates. DTB-specific gene expression and function are directed by cis-regulatory elements of developmental control genes that include homologs of mammalian Zinc finger of the cerebellum and Purkinje cell protein 4Drosophila DTB-specific cis-regulatory elements correspond to regulatory sequences of human ENGRAILED-2, PAX-2, and DACHSHUND-1 that direct MHB-specific expression in the embryonic mouse brain. We show that cis-regulatory elements and the gene networks they regulate direct the formation and function of midbrain circuits for balance and motor coordination in insects and mammals. Regulatory mechanisms mediating the genetic specification of cephalic neural circuits in arthropods correspond to those in chordates, thereby implying their origin before the divergence of deuterostomes and ecdysozoans.

Gene Regulatory Networks, Homology, and the Early Panarthropod Fossil Record.

The arthropod body plan is widely believed to have derived from an ancestral form resembling Cambrian-aged fossil lobopodians, and interpretations of morphological and molecular data have long favored this hypothesis. It is possible, however, that appendages and other morphologies observed in extinct and living panarthropods evolved independently. The key to distinguishing between morphological homology and homoplasy lies in the study of developmental gene regulatory networks (GRNs), and specifically, in determining the unique genetic circuits that construct characters. In this study, I discuss character identity and panarthropod appendage evolution within a developmental GRN framework, with a specific focus on potential limb character identity networks ("ChINs"). I summarize recent molecular studies, and argue that current data do not rule out the possibility of independent panarthropod limb evolution. The link between character identity and GRN architecture has broad implications for homology assessment, and this genetic framework offers alternative approaches to fossil character coding, phylogenetic analyses, and future research into the origin of the arthropod body plan.

ChINs, swarms, and variational modalities: concepts in the service of an evolutionary research program

Gunter Wagner’s Homology, Genes, and Evolutionary Innovation (2014) collects and synthesizes a vast array of empirical data, theoretical models, and conceptual analysis to set out a progressive research program with a central theoretical commitment: the genetic theory of homology. This research program diverges from standard approaches in evolutionary biology, provides sharpened contours to explanations of the origin of novelty, and expands the conceptual repertoire of evolutionary developmental biology (Evo–devo). I concentrate on four aspects of the book in this essay review: (1) the genetic theory of homology and character identity networks; (2) the implications for how we explain evolutionary novelties; (3) the expanded set of concepts surrounding homology, and (4) the epistemological conflicts between Wagner’s viewpoint and functionally-oriented evolutionary biology, as well as differences with other Evo–devo researchers. Together these have ramifications for how we interpret different explanatory approaches to evolutionary phenomena and understand relationships between the usefulness of concepts and the reality they represent.

Expression of a lung developmental cassette in the adult and developing zebrafish swimbladder.

The presence of an air-filled organ (AO), either lungs or a swimbladder, is a defining character of the Osteichthyes (bony vertebrates, including tetrapods). Despite the functional and structural diversity of AOs, it was not previously known whether the same group of developmental regulatory genes are involved in the early development of both lungs and swimbladders. This study demonstrates that a suite of genes (Nkx2.1, FoxA2, Wnt7b, GATA6), previously reported to be co-expressed only in the tetrapod lung, is also co-expressed in the zebrafish swimbladder. We document the expression pattern of these genes in the adult and developing zebrafish swimbladder and compare the expression patterns to those in the mouse lung. Early-acting genes involved in endoderm specification are expressed in the same relative location and stage of AO development in both taxa (FoxA2 and GATA6), but the order of onset and location of expression are not completely conserved for the later acting genes (Nkx2.1 and Wnt7b). Co-expression of this suite of genes in both tetrapod lungs and swimbladders of ray-finned fishes is more likely due to common ancestry than independent co-option, because these genes are not known to be co-expressed anywhere except in the AOs of Osteichthyes. Any conserved gene product interactions may comprise a character identity network (ChIN) for the osteichthyan AO.

Using Genetic Networks and Homology to Understand the Evolution of Phenotypic Traits

Homology can have different meanings for different kinds of biologists. A phylogenetic view holds that homology, defined by common ancestry, is rigorously identified through phylogenetic analysis. Such homologies are taxic homologies (=synapomorphies). A second interpretation, “biological homology” emphasizes common ancestry through the continuity of genetic information underlying phenotypic traits, and is favored by some developmental geneticists. A third kind of homology, deep homology, was recently defined as “the sharing of the genetic regulatory apparatus used to build morphologically and phylogenetically disparate features.” Here we explain the commonality among these three versions of homology. We argue that biological homology, as evidenced by a conserved gene regulatory network giving a trait its “essential identity” (a Character Identity Network or “ChIN”) must also be a taxic homology. In cases where a phenotypic trait has been modified over the course of evolution such that homology (taxic) is obscured (e.g. jaws are modified gill arches), a shared underlying ChIN provides evidence of this transformation. Deep homologies, where molecular and cellular components of a phenotypic trait precede the trait itself (are phylogenetically deep relative to the trait), are also taxic homologies, undisguised. Deep homologies inspire particular interest for understanding the evolutionary assembly of phenotypic traits. Mapping these deeply homologous building blocks on a phylogeny reveals the sequential steps leading to the origin of phenotypic novelties. Finally, we discuss how new genomic technologies will revolutionize the comparative genomic study of non-model organisms in a phylogenetic context, necessary to understand the evolution of phenotypic traits.

Why ontogenetic homology criteria can be misleading: lessons from digit identity transformations

As the basis for comparative biology, correctly assigning character homology is critical. Yet, identifying homologous characters in practice is often challenging. Among the major roadblocks is that the mechanistic bases of character homology remain in question. Thus, investigators must rely on several independent lines of evidence (e.g., character anatomy, phylogenetic distribution, or embryological position); however, these distinct sources of evidence often lead to conflicting diagnoses of character homology. What is more, there is no consensus regarding the relative importance of distinct lines of evidence for determining character homology. Here, we review the difficulties that have hindered the search for the mechanistic bases of character identity, and relate these issues to a recently proposed mechanistic hypothesis of character identity--the Character Identity Network Hypothesis. Next, using two well-studied cases of homology conflict (i.e., avian and skink digit identity), we assess the utility of different lines of evidence in diagnosing homology. We conclude that, when comparing adult structures, because anatomical characters more closely reflect the actions of the developmental genetic mechanisms of character individuation they are more reliable than embryological homology criteria.

The developmental genetics of homology

Homology is an essential idea of biology, referring to the historical continuity of characters, but it is also conceptually highly elusive. The main difficulty is the apparently loose relationship between morphological characters and their genetic basis. Here I propose that it is the historical continuity of gene regulatory networks rather than the expression of individual homologous genes that underlies the homology of morphological characters. These networks, here referred to as 'character identity networks', enable the execution of a character-specific developmental programme.