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

Amy R Mccune,John C Schimenti

doi:10.2174/138920212799034785

Abstract

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.

Highlights

The Genome Project in the 1990s and early 2000s was conducted in a very different technological era from today
Given the pervasive importance of homology for understanding biology and evolution, we review here how homology has been used differently by different kinds of biologists and show the commonality of these varied concepts of homology
In order to identify a Character Identity Networks (ChINs), a gene network must first be validated as a taxic homology and it must be homologous at the same phylogenetic level of inclusiveness as the phenotypic trait it is hypothesized to underlie

Summary

INTRODUCTION

The Genome Project in the 1990s and early 2000s was conducted in a very different technological era from today. Through the 20th century, the discipline of Genetics was essentially limited to a few model organisms –such as Escherichia coli, Saccharomyces cerevisiae, Drosophila melanogaster, and Mus musculus - around which biological and molecular infrastructure were accumulated over decades (such as mutations; specialized strains; genetic markers). These resources, coupled with both molecular biology tools that were developed in the latter quarter of the century, and the appearance of the first generations of automated DNA sequencers, enabled the genomic mapping and sequencing of these several organisms, plus humans. We discuss how the newest advances in genomic technology will further enhance our ability to expose the genetic basis for evolutionary change in (model and non-model) organisms

IMPLICIT AND EXPLICIT USES OF HOMOLOGY

ALTERNATIVE VIEWS OF HOMOLOGY

Phylogenetic or Taxic Homology

ChINs are taxic Homologies

ChINs Can Illuminate Phenotypic Transformation in a Comparative Context

CONCLUSIONS