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, F1s, 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 of biodiversity of mammals than is ‘‘reproductively isolated species.’’ Genetic profiles of mammalian species will result in a genetic description of species and mammalian diversity, and such studies are being accelerated by technological advances that reduce cost and increase speed and efficiency of generating genetic data. We propose that this genetic revolution remain museum- and voucher specimen‐based and that new names are based on a holotype (including associated tissues) deposited in an accredited museum.

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Speciation in mammals and the genetic species concept

Closely related species often differ karyotypically due to the fixation of chromosomal translocations and inversions which are generally deleterious when heterozygous but have normal fitnesses when homozygous (White, 1973; Muller, 1954, 1956). The fixation of such chromosomal rearrangements requires small population sizes, because they are selected against when in the minority but favored when in the majority, and hence they can become established in a local area only through random genetic drift. Naturalists have long known that most species exist in subdivided populations where each individual has a limited number of potential mates; and recent biogeographic studies, especially on islands, have emphasized the high turnover rates of local populations by extinction and colonization (Simberloff, 1974; Spight, 1974). The present paper develops population genetic models to determine how the fixation rates of negatively heterotic chromosomal rearrangements are influenced by the spontaneous occurrence rates, strengths of selection against heterozygotes, the effective size of demes (or local populations), interdeme migration rates, local extinction and colonization, and other factors. Data on chromosomal rearrangements concerning spontaneous occurrence, selection coefficients, and fixation rates in phylogeny are then used to draw inferences about the breeding structure of species during longterm evolution, particularly the effective size of demes. The effective size of a population through time, Ne, is the number of breed-

Effective deme sizes during long-term evolution estimated from rates of chromosomal rearrangement.

Parents divide their reproductive effort into the production of sons and daughters. Darwin (43) was intrigued by the fact that parents usually split their effort so that approximately equal numbers of sons and daughters are raised. He believed that this male: female ratio had been adjusted by natural selection because he understood that the number of females set a limit on reproductive capacity. He could not, however, clearly specify how natural selection shaped the sex ratio. Fisher (5 1 , 52) provided the explanation by noting that frequency-dependent selection stabilizes the sex ratio near equal­ ity. Since Fisher presented his explanation, many examples of biased sex ratios have been observed in nature. For example, Hamilton (7 1 ) observed very female-biased sex ratios in parasitic wasps that mate in small groups. Hamil­ ton explained this bias by showing that in these wasps the mating competition among brothers violates a latent assumption in Fisher's argument. In other examples of observed biases, the explanations put forth provided new dimensions to Fisher's central theory rather than direct exceptions. The most important of these new dimensions for birds and mammals was observed by Trivers & Willard (109). They noted that, in some mammals, healthy mothers tended to produce a relatively higher proportion of sons than did unhealthy mothers. They explained this pattern of variation among families

/pdf/sex-allocation-theory-for-birds-and-mammals-3ansab6bop.pdf

Sex Allocation Theory for Birds and Mammals

Unisexual hybrid disruption can be accounted for by interactions between sex ratio distorters which have diverged in the species of the hybrid cross. One class of unisexual hybrid disruption is described by Haldane's rule, namely that the sex which is absent, inviable or sterile is the heterogametic sex. This effect is mainly due to incompatibility between X and Y chromosomes. We propose that this incompatibility is due to a mutual imbalance between meiotic drive genes, which are more likely to evolve on sex chromosomes than autosomes. The incidences of taxa with sex chromosome drive closely matches those where Haldane's rule applies: Aves, Mammalia, Lepidoptera and Diptera. We predict that Haldane's rule is not universal but is correct for taxa with sex chromosome meiotic drive. A second class of hybrid disruption affects the male of the species regardless of which sex is heterogametic. Typically the genes responsible for this form of disruption are cytoplasmic. These instances are accounted for by the release from suppression of cytoplasmic sex ratio distorters when in a novel nuclear cytotype. Due to the exclusively maternal transmission of cytoplasm, cytoplasmic sex ratio distorters cause only female-biased sex ratios. This asymmetry explains why hybrid disruption is limited to the male.

https://www.genetics.org/content/genetics/128/4/841.full.pdf

Causes of Sex Ratio Bias May Account for Unisexual Sterility in Hybrids: - a New Explanation of Haldane's Rule and Related Phenomena

The karyotypes of more than 60 species of Primates are studied and compared, with the use of almost all existing banding techniques. There is a very close analogy of chromosome banding between the Simians studied and man. The quantitative or qualitative variations detected all involve the heterochromatin. It is very likely that all the euchromatin (nonvariable R and Q bands) is identical in all the species. Approximately 70% of the bands are common to the Simians and to the Lemurs (Prosimians). In the remaining 30%, technical difficulties prevented a valuable comparison, but this does not exclude the possibility that a complete analogy may exist. Thus, it is very likely that chromosomal evolutions of the Simians, and probably of all the Primates, has occurred without duplication or deficiency of the euchromatin. Approximately 150 rearrangements could be identified and related to the human chromosomes. The types of rearrangements vary from one group (suborder, family, genus) to another. For instance, Robertsonian translocations are preponderant among the Lemuridae (44/57) but are nonexistent among the Pongidae. Chromosome fissions are very frequent among the Cercopithecidae (10/23), but were not found elsewhere, and pericentric inversions are preponderant in the evolution of Pongidae and man (17/28). This suggests that the chromosomal evolution may be directed by the genic constitution (favouring the occurrence of a particular type of rearrangement, by enzymatic reaction), by the chromosomal morphology (the probability that Robertsonian translocations will be formed depends at least partially on the number of acrocentrics), and by the reproductive behaviour of the animals. Reconstitution of the sequence of the chromosomal rearrangements allowed us to propose a fairly precise genealogy of many Primates, giving the positions of the Catarrhines, the Platyrrhines, and the Prosimians. It was also possible to reconstruct the karyotypes of ancestors that died out several dozen million years ago. The possible role of chromosomal rearrangements in evolution is discussed. It appears necessary to consider different categories of rearrangements separately, depending on their behaviour. The ‘nonfavoured’ rearrangements, such as pericentric inversions, need to occur in an isolated small population for implanting, by an equivalent of genic derivation. The ‘favoured’ rearrangements, e.g., Robertsonian translocations, may occur and diffuse in panmictic populations, and accumulate. Their role of gametic barrier could be much more progressive. For discrimination between these two categories, it was necessary to differentiate the selective advantage or disadvantage of the rearrangement itself. It was not possible to show that chromosomal rearrangements play a direct role in modification of the phenotype by position effect. Comparison of the rearrangements that have occurred during evolution and those detected in the human population shows a strong correlation for some of them. In particular, a large proportion of pericentric inversions can be regarded as reverse mutations, because they reproduce ancestral chromosomes.

Chromosomal evolution in primates: tentative phylogeny from Microcebus murinus (Prosimian) to man.

A survey is given on the occurrence, the geographic origin and the arm composition of 27 Robertsonian fusion metacentric chromosomes of wild populations of the mouse. Their study is of twofold interest: a) it is possible to introduce these naturally occurring metacentrics in laboratory strains for experimental use. At present, altogether 34 metacentric chromosomes of different composition are available including 7 cases of metacentrics known from laboratory strains of the mouse. b) With the search for metacentrics in the mouse and with their identification insights are permitted in the role of Robertsonian changes in the course of mammalian evolution — Several separate populations of the mouse with different sets of multiple (up to 9) metacentrics have been found in Switzerland and Italy. Some of the individual metacentrics may occur in different populations. The participation of an acrocentric autosome in the formation of metacentrics seem to be at random, but the sex chromosomes are never included in a metacentric. — Homology of the arms involved in metacentrics is conserved, so that in meiosis of interpopulation hybrids long chains or rings are observed. They may include up to 16 metacentrics arranged according to the alternating homologies of their arms. — Reduction of fertility of single or multiple metacentric heterozygotes and of the interpopulation hybrids is due to mechanisms of segregational imbalance and subsequent prenatal elimination of fetal offspring, but it follows also the pattern of male limited hybrid sterility. — From an evolutionary view point, karyotype rearrangements of Robertsonian type may initiate reproductive isolation, which prepares the ground for further genetic diversification and, as in the case of the mouse, of incipient speciation.

Robertsonian metacentrics in the mouse.

The European longtailed house mouse (M. m. brevirostris and domesticus) in the Rhaetian Alps and Lombardia presents a complex system of Robertsonian (Rb) variation and karyotype diversity, several adjoining populations homozygous for multiple Rb metacentric chromosomes, sites of coexistence of different Rb types, and zones of hybridization with non-Rb populations. The original "tobacco mouse" is just one of many local Rb variants, such as those from other Alpine areas (e.g., Orobian Alps) or from Central Lombardia, where a relatively large region within which the population is homogeneous for multi-Rb metacentrics is found. The present study is based strictly on material in which the chromosome arms were identified by G-banding, so that karyotypes within the areas under investigation could be compared. Altogether 111 mice were studied.

Robertsonian karyotype variation in wild house mice from Rhaeto-Lombardia.

The wood lemming displays certain peculiar features: (1) The sex ratio shows a prevalence of females (FRANK, 1966; KALELA and OKSALA, 1966), and some females produce only female offspring (KALELA and OKSALA, 1966). (2) In a considerable proportion (in the present material, slightly less than half) of the females, an XY chromosome complement is found in the somatic tissues, but the Y is absent in the germ line of those studied (Fredga et al., 1976). Therefore, (3) a mechanism of double nondisjunction in early fetal life of XY females has to be postulated, which replaces the Y in the germ line by duplication of the X. It is assumed (4) that the X of XY females bears a sex-reversal factor that affects the male determining action of the Y (Fredga et al., 1977). There is (5) a strong presumption that in most cases the XY females are those that produce daughters only, but (6) a few exceptions may occur (FRANK, unpublished observations), suggesting that the regulation according to assumption 3 (perhaps also to 4) is incomplete in XY females. In the present report, four females are described with a 31,XO karyotype, two females with 33,XYY or 32,XY/33,XYY, respectively, two males with a 33,XXY, and one male with a 32,XX/33,XXY karyotype, as observed in a consecutive series of 502 wood lemmings. The incidence of sex-chromosome anomalies in liveborn and adult animals was 2.3%; the overall incidence, including embryos, was 1.79%. Neither the somatic XO constitution nor the existence of an extra Y in females precludes fertility. However, the XXY condition in the male results in sterility. There is certain evidence that an instability of the proposed mechanism for double mitotic nondisjunction of the sex chromosomes in oogonia accounts for the high rate of sex-chromosome aberrations in wood lemmings, at least when the mother is XY.

G. Noack

Papers

Robertsonian metacentrics in the mouse.

Robertsonian karyotype variation in wild house mice from Rhaeto-Lombardia.

Sex-chromosome aberrations in wood lemmings (Myopus schisticolor).