The avian world is packaged into genetic assemblages that we call species. Although ornithologists can, with a few important exceptions, agree on the boundaries among avian gene pools that delimit species, the evolutionary process that created this structured subdivision of Aves remains uncertain and contentious. Moreover, although avian species are recognizable and diagnosable, many bear signatures of recent, often substantial, exchange of nuclear (N) genetic material. As a result, there is debate regarding the process that gives rise to and maintains the genetic structure of avian populations. I propose that a key missing consideration in discussions of speciation is the necessity of coadaptation between N and mitochondrial (mt) genes to enable core energy production via oxidative phosphorylation. Because mt genomes are non-recombining and subject to high mutation rates, they evolve rapidly. Consequently, N and mt coadaptation persists only through perpetual coevolution between mt and N genes. Mitonuclear coevolution leads to rapid divergences in coadapted mitonuclear gene sets whenever there is a disruption in gene flow among populations. As a result, once populations diverge in coadapted mitonuclear genotypes, the reduced fitness of offspring due to mitonuclear incompatibilities prohibits exchange of mt and N-mt genes and effectively isolates individuals with shared coadapted N and mt genotypes. Given these considerations, I propose that avian species can be objectively diagnosed by uniquely coadapted mt and N genotypes that are incompatible with the coadapted mt and N genotype of any other population. According to this mitonuclear compatibility species concept, mitochondrial genotype is the best current method for diagnosing species.
In the early 20th century, Ernst Mayr, the great avian biogeographer and evolutionary theorist, grappled with the question of whether avian species are real biological entities or simply a fabrication of western taxonomists (Mayr 1940). He made a compelling case that avian species are real and can be objectively and repeatably delineated. The species concept articulated by Mayr and endorsed by the American Ornithologists' Union (AOU) Committee on Classification and Nomenclature is that “species are genetically cohesive groups of populations that are reproductively isolated from other such groups” (AOU 1998). Thus, there is at least some consensus that species are more-or-less discrete gene pools (Gill 2014, Toews 2015). A rapidly expanding literature on the genetic structure of populations, however, indicates that gene flow is common among populations recognized as species—and sometimes substantial between populations unanimously recognized as species (e.g., Toews et al. 2016b). In most birds, this flow of genes appears to be much greater for autosomal genes than for sex-linked or mitochondrial (mt) genes (Carling and Brumfield 2008, Qvarnström and Bailey 2009, Rheindt and Edwards 2011). The paradox of avian taxonomy in the early twenty-first century is that the more we learn about the genetic structure of populations, the more current theories of speciation become inadequate to explain the observed patterns (Harrison and Larson 2014).
In this essay, I present an argument that species are best defined by coadapted sets of mt and nuclear (N) genes. In presenting this new species concept, I make no attempt to comprehensively review the hundreds of papers and several books that have been written on animal and avian speciation. The state of thought regarding avian speciation and the concept of species as applied to birds was thoroughly summarized by Gill (2014) and Toews (2014), and empirical studies of avian speciation were comprehensively reviewed by Price (2007). I present only a brief overview of dominant current models of speciation in order to provide necessary context for the proposed model. Mitonuclear coadaptation was not mentioned in any recent treatments of avian species concepts, so my primary goal here is to introduce the ornithological community to the concepts of mitonuclear coadaptation and coevolution as central to understanding the process of speciation and the nature of avian species.
I present my argument for mitonuclear genomic interactions driving speciation specifically in birds—rather than all vertebrates, metazoans, or eukaryotes—because, as an ornithologist, I can articulate and assess a mitonuclear compatibility hypothesis of speciation most effectively in birds. Ornithologists have played a dominant role in the development of species concepts because birds are by far the best-known animal taxon (Scheffers et al. 2012). Birds are typically diurnal and conspicuous, so ornithologists had recorded the phenotypes (particularly coloration and song) as well as the distributions of the great majority of the world's bird populations by the early twentieth century (Sharpe 1909, Mayr 1970). While humans cannot perceive the signals used in species recognition by most animal species (Palumbi 1994), the primary sensory modalities of birds are the same used by humans, so sounds and morphological features that are conspicuous to birds—and potentially important in distinguishing conspecifics from heterospecifics—are also apparent to humans (Hill 2006). For many decades, ornithologists stood on the platform of their knowledge of the biogeography of Aves as they speculated on the processes that gave rise to this biodiversity and debated where species boundaries should be drawn (Mayr 1940, 1982, Cracraft 1983, Zink and McKitrick 1995). If an argument can be made for the importance of mitonuclear coadaptation in avian speciation, then the full scope of the theory can be explored through extrapolation to other taxa.
The mitonuclear compatibility model of speciation requires a basic understanding of how products of the mt genome and products of the N genome co-function to create oxidative phosphorylation (OXPHOS), so I begin with a brief review of the genomic architecture of the electron transport system (ETS) and a discussion of how this architecture necessitates tight mitonuclear coadaptation that can be maintained only through perpetual mitonuclear coevolution. I then present the mitonuclear compatibility model of speciation in detail. I conclude by applying this mitonuclear perspective to the interpretation of patterns of (1) distinctiveness of mt genotypes between avian populations; (2) greater introgression of autosomal vs. mt or sex-linked genes between putative avian species; (3) chromosomal locations of genes for ornamentation, preference, and incompatibility; (4) disproportionate effects of hybridization on the heterogametic sex (Haldane's rule); and (5) hybrid speciation in birds.
Mitonuclear Coadaptation: A Missing Fundamental Principle in Concepts of Speciation
For a eukaryote to be a functional organism, it must have coadapted mt and N genes (Rand et al. 2004,