Speciation in Mammals and the Genetic Species Concept

Abstract

We define a genetic species as a group of genetically compatible interbreeding natural populations that is genetically isolated from other such groups. This focus on genetic isolation rather than reproductive isolation distinguishes the Genetic Species Concept from the Biological Species Concept. Recognition of species that are genetically isolated (but not reproductively isolated) results in an enhanced understanding of biodiversity and the nature of speciation as well as speciation-based issues and evolution of mammals. We review criteria and methods for recognizing species of mammals and explore a theoretical scenario, the Bateson-Dobzhansky-Muller (BDM) model, for understanding and predicting genetic diversity and speciation in mammals. If the BDM model is operating in mammals, then genetically defined phylogroups would be predicted to occur within species defined by morphology, and phylogroups experiencing stabilizing selection will evolve genetic isolation without concomitant morphological diversification. Such species will be undetectable using classical skin and skull morphology (Morphological Species Concept). Using cytochrome-b data from sister species of mammals recognized by classical morphological studies, we estimated the number of phylogroups that exist within mammalian species and hypothesize that there will be >2,000 currently unrecognized species of mammals. Such an underestimation significantly affects conclusions on the nature of speciation in mammals, barriers associated with evolution of genetic isolation, estimates of biodiversity, design of conservation initiatives, zoonoses, and so on. A paradigm shift relative to this and other speciation-based issues will be needed. Data that will be effective in detecting these "morphologically cryptic genetic species" are genetic, especially DNA-sequence data. Application of the Genetic Species Concept uses genetic data from mitochondrial and nuclear genomes to identify species and species boundaries, the extent to which the integrity of the gene pool is protected, nature of hybridization (if present), and introgression. Genetic data are unique in understanding species because the use of genetic data 1) can quantify genetic divergence from different aspects of the genome (mitochondrial and nuclear genes, protein coding genes, regulatory genes, mobile DNA, microsatellites, chromosomal rearrangements, heterochromatin, etc.); 2) can provide divergence values that increase with time, providing an estimate of time since divergence; 3) can provide a population genetics perspective; 4) is less subject to convergence and parallelism relative to other sets of characters; 5) can identify monophyly, sister taxa, and presence or absence of introgression; and 6) can accurately identify hybrid individuals (kinship and source of hybrid individuals, F(1)s, backcrosses, direction of hybridization, and in concert with other data identify which hybrids are sterile or fertile). The proposed definition of the Genetic Species Concept is more compatible with a description o...

A new species of small-eared shrew (Mammalia, Eulipotyphla,Cryptotis) from the Lacandona rain forest, Mexico

“…The average genetic distances between other sister species of Cryptotis (sensu Guevara and Cervantes 2013) range from 2.0% to 6.8% (Table 3; e.g., C. magnus and C. phillipsii, 6.8%; C. mexicanus and C. obscurus, 5.1%; C. goldmani and C. peregrinus, 2.0%). Small (, 5%) genetic distances are known for other closely related species of mammals that had been recognized on the basis of morphology before use of molecular approaches (see Baker and Bradley 2006). The genetic distances support our morphological result in allying the Lacandona shrew most closely with the C. nigrescens species group rather than either the C. mexicanus or C. parvus groups.…”

Natural hybridization generates mammalian lineage with species characteristics

“…Furthermore, our maximum estimate of the TMRCA among these species is ∼3.5 Mya, a value younger than the hypothesized rate of hybrid inviability for mammals (18,41). The patterns of differential rates of reproductive isolation in allopatry described above are compatible with theoretical models of speciation (18,42,43). Theoretical treatments of hybrid speciation have shown that speciation is likely to occur faster when the chromosomal differences between the parental taxa were low and the hybrids were common in a given population (44).…”

Niche conservatism above the species level

“…We recognize that in some kinds of animals and many kinds of plants, the grouping of ''genus'' and ''family'' may not reflect monophyletic groups; thus, we confine our analysis to mammals, in which these ranks typically do reflect monophyly and aggregate similar evolutionary distances (27)(28)(29). We focus on mammals, because there is little disagreement that most genera are monophyletic and do in fact reflect a real evolutionary grouping, although we of course recognize some may object to even using the term ''genus'' in view of current phylogenetic practice.…”

“…Most mammal species in North America are significantly older than 130,000 years. In fact, the mean divergence between North American sister species (within genera) is at least an order of magnitude older (27,28,34). Thus, we predict that the intrinsic traits (e.g., trait-based controls on geographic range) that define range size in these animals evolved before the LP glacial-interglacial cycles and, accordingly, we anticipate that the relative range sizes will remain fairly constant, simply because North American mammalian species have witnessed repeated glacial-interglacial cycles in their lifespan (as many as 18 cycles; ref.…”