Giora Heth

Adaptive optimal sound for vocal communication in tunnels of a subterranean mammal (Spalax ehrenbergi)

The adaptive value of sound signal characteristics for transmission in the underground tunnel ecotope was tested using tunnels of the solitary territorial subterranean mole rats. We analyzed the propagation of synthetic calls with various frequencies through natural tunnels along different distances. Here we present evidence that sound propagation proved efficient only across short distances (a few meters). The least attenuation of sounds occurred at low frequencies. The 440 Hz sound was transmitted better than the lower (220 Hz) or higher (880, 1760, 3520 Hz) tested frequencies. These characteristics matched perfectly with the mole rat features of vocalization and hearing, thus reflecting the operation of natural selection for adaptive vocal communication in the underground tunnel ecotope.

Odor–Genes Covariance and Genetic Relatedness Assessments: Rethinking Odor-Based “Recognition” Mechanisms in Rodents

Publisher Summary This chapter presents the findings that led to the reevaluation of mechanisms underlying differential responses to odors including a description of the methodologies used to collect the data. The chapter suggests new ways of interpreting the terms used in describing discriminative responses to odors and proposes a hypothesis about the origin and evolutionary basis of differential responses based on genetic relatedness assessments. Prospects for future studies that could deepen the understanding of how these mechanisms work are discussed in detail. The chapter presents data based on the responses of rodents to odors and explores the principles in the experiments that apply equally well to other taxa and to sensory modalities other than olfaction, particularly vision and audition. There were two important consequences of the studies for understanding recognition mechanisms: (1) differential responses to odors of familiar and unfamiliar individuals indicated that rodents learn to associate particular individuals with their individual odors and can recognize the odors of familiar individuals irrespective of genetic relatedness, thus “individual recognition” is a mechanism for responding both to kin and nonkin rather than a “kin recognition” process; (2) in conjunction with evidence for self-referencing in graded responses based on degrees of genetic relatedness to odors of kin, populations, and species, the odor–genes covariance findings raised the intriguing possibility that such self-referencing would be the most practical means of assessing degrees of genetic relatedness to any other individual.

Vibrational communication in subterranean mole rats (Spalax ehrenbergi)

SummaryWe describe a vibrational communication system in subterranean mole rats of the Spalax ehrenbergi superspecies in Israel. The signals are produced by head thumping against the tunnel ceiling in a rhythmic pattern that appears to be species-specific. These signals may be effective as a means of long-distance communication between individuals within populations, as well as acting as a pre-mating isolating mechanism between populations in the final stages of speciation.

Karyotype and genetic evolution in speciation of subterranean mole rats of the genus Spalax in Turkey

Karyotype (2n) and allozyme diversity at 37 gene loci were determined in 69 subterranean mole rats in Turkey belonging to the two superspecies: the ancestor Spalax leucodon (n = 55; 20 populations) and the descendant S. ehrenbergi (n = 14: four populations. We identified remarkable variation of diploid chromosome numbers in the S. leucodon superspecies: 2n = 38, 40, 50, 54, 60 and 62; and in the S. ehrenbergi superspecies: 2n = 52, 56 and 58. Genetic diversity indices were low on average in both S. leucodon and S. ehrenbergi superspecies: Allele diversity, A = 1.081 and 1.074; polymorphism, P-50 0 = 0.077 and 0.068; heterozygosity, H = 0.038 and 0.027; and gene diversity, H = 0.038 and 0.034, respectively. H ranged from 0 in mesic or semimesic regions to 0.088 in arid Anatolia. We consider the populations with different diploid chromosome numbers, 2n, as good biological species. Karyotypic diversity may mark extensive ecological speciation. Nees genetic distances, D average 0.174, range 0.002 0.422) and ecogeographical criteria suggest that almost each population may represent a different biological species, but critical future testing is necessary to support this claim. Karyotypes and allozymes are nonrandomly distributed across Turkey, displaying remarkable correlations with climatic and biotic factors. Both 2n and H are significantly correlated with aridity stress (2n/rainfall. r = −0.74; P < 0.001), and in our region also with climatic unpredictability. These results support the niche-width genetic variation hypothesis in space and time. Climatic selection in Turkey appears to be a major architect of karyotype and genetic (allozyme) diversity and divergence in mole rat evolution, in both speciation and adaptation.

Olfactory discrimination as an isolating mechanism in speciating mole rats

Olfactory discrimination was tested in two chromosome forms of the speciating fossorial rodent,Spalax ehrenbergi, in Israel. Females of the chromosome forms 2n=52 and 2n=58 were tested for male odour discrimination, the source of odour being either cage litter or urine. Estrous females of both forms preferred homochromosomal odours, whereas diestrous females showed no discrimination. These results suggest that olfactory discrimination may serve as a reproductive isolating mechanism in the speciation of mole rats.

Effects of in utero odorant exposure on neuroanatomical development of the olfactory bulb and odour preferences

Human babies and other young mammals prefer food odours and flavours of their mothers diet during pregnancy as well as their mothers individually distinctive odour. Newborn mice also prefer the individual odours of more closely related—even unfamiliar—lactating females. If exposure to in utero odorants—which include metabolites from the mothers diet and the foetuss genetically determined individual odour—helps shape the neuroanatomical development of the olfactory bulb, this could influence the perception of such biologically important odours that are preferred after birth. We exposed gene-targeted mice during gestation and nursing to odorants that activate GFP-tagged olfactory receptors (ORs) and then measured the effects on the size of tagged glomeruli in the olfactory bulb where axons from olfactory sensory neurons (OSNs) coalesce by OR type. We found significantly larger tagged glomeruli in mice exposed to these activating odorants in amniotic fluid, and later in mothers milk, as well as significant preferences for the activating odour. Larger glomeruli comprising OSNs that respond to consistently encountered odorants should enhance detection and discrimination of these subsequently preferred odours, which in nature would facilitate selection of palatable foods and kin recognition, through similarities in individual odours of relatives.

ORIGIN AND EVOLUTION OF ETHOLOGICAL ISOLATION IN SUBTERRANEAN MOLE RATS

Reproductive isolation is essential for speciation and for the maintenance of species genetic integrity, yet its origin and evolution, particularly of ethological isolation, is still largely controversial and in most cases unknown (Mayr, 1970). The nature, origin and evolution of reproductive isolation may be highlighted particularly in actively evolving species, and thereby contribute to understanding the process of speciation and the evolutionary future of hybrid zones between parapatric species. There are two major classical theories of the origin of isolating mechanisms (Mayr, 1970; Dobzhansky et al., 1977): (a) the allopatric, or incidental origin theory and (b) the sympatric, or reinforcement theory. According to the former, pre-zygotic isolating mechanisms arise as an incidental by-product of genetic divergence in isolated populations (Darwin, 1859; Muller, 1940, 1942; Mayr, 1942, 1970). The latter theory postulates that isolating mechanisms are perfected through direct selection when two incipient species begin to become sympatric, through progressive elimination of hybrids of lower fitness, in the overlapping (sympatric) zones (Wallace, 1889; Fisher, 1930; Dobzhansky, 1940, 1970). It is widely accepted that post-zygotic isolating mechanisms are the incidental result of evolutionary divergence (Moore, 1957; Littlejohn, 1969; Dobzhansky et al., 1977; but see also alternative views in Grant, 1966; Watson and Martin, 1968; Coyne, 1974). The main controversy between the allopatric and sympatric theories concerns the origins of pre-zygotic isolating mechanisms, and is focused on the question of the extent to which direct selection contributes to this acquisition. The problem may be restated as follows: is the pre-zygotic isolation accumulated and perfected strictly as an incidental by-product of divergence in isolated populations-or, do these mechanisms evolve primarily by direct selection in sympatry (Dobzhansky, 1970; Dobzhansky and Pavlovsky, 1971; Ehrman, 1971, 1979). A third alternative combines the two theories suggesting that the principal genetic basis of this isolation was acquired in separate gene pools and then perfected by direct selection in sympatry. The studies and techniques which support the allopatric theory have been extensively reviewed (Grant, 1966, 1977; Littlejohn, 1969, 1980; Mayr, 1970; Brown, 1975), but only in a small number of cases was there clear experimental evidence for this process (e.g., Nevo, 1969b; Capranica et al., 1973). A much larger number of experiments studied the reinforcement process, and results of these studies are generally interpreted as supporting this theory (see the above reviews and also Dobzhansky, 1970; Blair, 1974; Dobzhansky et al., 1977). Yet critical analysis of these studies reveal that only a few of them provide unequivocal evidence for reinforcement in pre-zygotic isolation (see reviews of different taxa in Thielcke, 1973; Walker, 1974; Fouquette, 1975; Loftus-Hills, 1975). Therefore, critical tests of the origin of pre-zygotic isolation are indispensable in as large of array of taxa as possible. Suitable methodologies for such studies are suggested and discussed by Grant (1966), Littlejohn (1969), and Nevo (1969b). Recently, an additional, chiefly stochastic theory of the origin of pre-zygotic isolating mechanisms has been suggested (Carson, 1975, 1978; Kaneshiro, 1976).

Hematocrit and hemoglobin concentration in four chromosomal species and some isolated populations of actively speciating subterranean mole rats in Israel.

Hematocrit (HCT) and hemoglobin (Hb) concentration were measured in four chromosomal species and some peripherally semi-isolated and isolated populations of the mole rat superspeciesSpalax ehrenbergi in Israel. HCT was 52.0, 51.4, 50.9, and 47.8%, and Hb was 16.0, 16.6, 16.3, and 14.7 g/100 ml for 2n=52, 58, 54, and 60, respectively. The species 2n=60, which lives in arid habitats, had lower HCT and Hb than the other three species. HCT decreased as aridity increased between the species and within the species 2n=60. Changes in HCT probably reflect clinal changes in both soil permeability to gases and ambient temperature.

Assortative mating between chromosome forms of the mole rat,Spalax ehrenbergi

Females of two parapatric chromosomal forms (2n=52 and 2n=58) of the fossorial mole rat,Spalax ehrenbergi, in Israel, were tested for mate selection between two alternative, a homo- and a heterochromosomal, males. Estrous females significantly preferred the male of their own chromosomal form, on the basis of several behavioural criteria. The evolutionary significance of the positive assortative mating found, lies presumably in reinforcing reproductive isolation between the chromosome forms, thereby contributing to finalize speciation.

Aggression patterns in adaptation and speciation of subterranean mole rats

The patterns and correlates of aggressionwithin andbetween actively speciating subterranean mole rats of theSpalax ehrenbergi superspecies in Israel were tested in an attempt to approach an evolutionary theory of aggression related to both adaptation and speciation. Laboratory experiments were conducted on 314 adult mole rats (188 males and 126 females) caught in nature, representing 12 populations and comprising four chromosomal species (2n = 52, 54, 58, 60). The present analysis concentrates on “total aggression” comprising four aggressive variables: attacks, bitings, head-ons and sniffing with open mouth, out of 23 recorded variables. The results indicate that (a) aggression is distributed as a multipeak, discontinuous phenotypic parameter, displaying polymorphism within all 12 populations and 4 species tested; (b) the level of aggression was higher in males than in females, in the breeding than in the nonbreeding season, and displayed clinal geographic variation in both sexes across the superspecies range, where “militancy” increased northwards; (c) aggression was significantly correlated with ecological, physiological, genetical and ethological factors. These results support an evolutionary theory of aggression related to the intertwined processes of adaptation and speciation.