Brain size diversity in adaptation and speciation of subterranean mole rats

We have tested brain size diversity and encephalization in the actively speciating subterranean mole rats of the Spalax ehrenbergi superspecies in Israel. Our sample involved 171 individuals comprising 12 populations and 4 chromosomal species (2n = 52, 54, 58 and 60) distributed parapatrically from the northern Mediterranean region southward (2n = 52, 54→+58→60) into increasingly more arid and unpredictable climatic regimes, approaching the Negev Desert. Our results indicate that relative brain size and encephalization are highest in 2n = 60 as compared with 2n = 52, 54 and 58. We hypothesize that this pattern is adaptive and molded by natural selection. Brain evolution and higher encephalization in the S. ehrenbergi complex appears to be associated with increasing ecological stresses of aridity and climatic unpredictability.     

MtDNA polymorphisms: evolutionary significance in adaptation and speciation of subterranean mole rats

Patterns of mtDNA diversity in subterranean mole rats of the Spalax ehrenbergi superspecies (2n = 52, 54, 58 and 60) were previously studied in the main ranges of the four chromosomal species, and specifically in the 2n = 60 species and its peripheral steppe semi-isolates and desert isolates. In the present study we correlated mtDNA diversity indices, nucleon diversity, h , and nucleotide divergence, π, with physical (climatic), biotic (parasites) and biological (genetical, morphological, physiological and behavioural) factors, showing that mtDNA diversity is structured ecogeographically and biologically. The following significant correlations of mtDNA diversity were indicated with: (i) climatic heterogeneity and unpredictability; (ii) levels of ecto- and endoparasites; and (iii) biological diversities, primarily with physiological diversity associated with the energy budget. Small steppe semi-isolates and desert isolates harbour high levels of mtDNA haplotype diversity, some novel, which may be a prerequisite for future speciation events. We conclude that the ecogeographical and biological correlates, as well as the maintenance of mtDNA polymorphisms in small isolated populations, strongly suggest that mtDNA diversity is not neutral. Diversifying natural selection appears to be an important differentiating factor of mtDNA diversity in the twin evolutionary processes of adaptive radiation and active speciation. We suggest critical experiments to substantiate our conclusions and highlight the contribution of mtDNA diversity to fitness, i.e. to the biological function of mtDNA diversity in the evolutionary process.     

Brain organization and evolution in subterranean mole rats

Relative brain component sizes have been analyzed in subterranean mole rats of the Spalax ehren-bergi superspecies in Israel. Our results indicate that brain size and brain component sizes may have evolved in association with specific stresses underground involving the distinct development of vocalzation, olfaction and tactile sensory communication systems all compensating for the loss of vision.     

Morphometrics of speciating mole rats: Adaptive differentiation in ecological speciation

The morphometrics of subterranean mole rats, Spalax ehrenbergi superspecies in Israel, were studied. A total of 42 skull and body variables of 327 adults from 44 populations across the ranges of the 4 chromosomal species (2n = 52, 54, 58 and 60) were measured. The results showed: a. in general, significantly higher morphological values in males than in females; b. significant interspecific quantitative diffferences in 15 skull variables of males, and in 3 of females; but no qualitative diagnosis of any of the species; c. an intercorrelation between most skull variables at different orgamsmal levels, and a uniform and complete correlation with weight; d. a statistical discrimination in both metric and nonmetric multivariate analyses between most species pairs; e. an indication of high morphological similarity based on the relatively small multivariate Mahalanobis distances of dissimilarity between species; f. a possible explanation for a significant part of the variance in most skull and body variables resulting from a combination of temperature variables and water availability; g. a declination in size in skull and body variables between northern and southern species; h. the order of speciation events to be 2n = (54, 52)→58→60. Based on these results we conclude: 1. no morphological breaks are associated with the speciation of the S. ehrenbergi complex, and morphological differentiation is quantitative rather than qualitative between the species: 2. morphological diversity is significantly explained by climatic selection, and is therefore adaptive and explicable on even very low selective pressures over evolutionary time: 3. the morphospecies seem unable to reliably reflect the biological species in the S. ehrenbergi complex, and morphological differentiation, at least in this superspecies, evolves in a gradual rather than a punctual way: this would conform with Neo-Darwinian evolutionary theory.     

Sexual size dimorphism and selection in the wild in the waterstrider Aquarius remigis: Body size,components of body size and male mating success

Sexual size dimorphism is assumed to be adaptive and is expected to evolve in response to a difference in the net selection pressures on the sexes. Although a demonstration of sexual selection is neither necessary nor sufficient to explain the evolution of sexual size dimorphism, sexual selection is generally assumed to be a major evolutionary force. If contemporary sexual selection is important in the evolution and maintenance of sexual size dimorphism then we expect to see concordance between patterns of sexual selection and patterns of sexual dimorphism. We examined sexual selection in the wild, acting on male body size, and components of body size, in the waterstrider Aquarius remigis, as part of a long term study examining net selection pressures on the two sexes in this species. Selection was estimated on both a daily and annual basis. Since our measure of fitness (mating success) was behavioral, we estimated reliabilities to determine if males perform consistently. Reliabilities were measured as ? statistics and range from fair to perfect agreement with substantial agreement overall. We found significant univariate sexual selection favoring larger total length in the first year of our study but not in the second. Multivariate analysis of components of body size revealed that sexual selection for larger males was not acting directly on total length but on genital length. Sexual selection for larger male body size was opposed by direct selection favoring smaller midfemoral lengths. While males of this species are smaller than females, they have longer genital segments and wider forefemora. Patterns of contemporary sexual selection and sexual size dimorphism agree only for genital length. For total length, and all other components of body size examined, contemporary sexual selection was either nonsignificant or opposed the pattern of size dimporhism. Thus, while the net pressures of contemporary selection for the species may still act to maintain sexual size dimorphism, sexual selection alone does not.     

DNA sequence variation in the mitochondrial control region of subterranean mole rats,Spalax ehrenbergi superspecies,in Israel

The complete mitochondrial control region was sequenced for 60 individuals representing different populations for each of the four species of the subterranean mole rat Spalax ehrenbergi superspecies in Israel: Spalax galili (2n = 52), S. golani (2n = 54), S. carmeli (2n = 58), and S. judaei (2n = 60). The control region of all species and populations is very similar both in length (979 to 983 bp) and in base composition. As in agreement with previous surveys on mitochondrial control regions on mammals, the mole rat control region can be divided into a central domain and two flanking domains, ETAS (extended termination associated sequences) and CSB (conserved sequence blocks). Along with the common conserved blocks found in these domains (ETAS1, ETAS2, CSB1, CSB2, and CSB3), we have also detected in all individuals an ETAS1-like and a CSB1-like element, both in the ETAS domain. The most conserved region was the central domain, followed by the CSB and ETAS domains, showing important differences in the four species analyzed. Phylogenetic analysis supported the existence of two clades. One clade contained individuals belonging to Spalax galili (2n = 52) and S. golani (2n = 54), separated in two different branches depending on the species. The other clade contained individuals belonging to S. carmeli (2n = 58) and S. judaei (2n = 60) mixed together, suggesting a more recent event of speciation. Within species we have observed a southward trend of increasing variability. These results have been explained as a consequence of the adaptation of the species to ecological factors such as aridity and temperature stresses.     

Sexual selection and sexual size dimorphism in animals

Sexual selection is often considered as a critical evolutionary force promoting sexual size dimorphism (SSD) in animals. However, empirical evidence for a positive relationship between sexual selection on males and male-biased SSD received mixed support depending on the studied taxonomic group and on the method used to quantify sexual selection. Here, we present a meta-analytic approach accounting for phylogenetic non-independence to test how standardized metrics of the opportunity and strength of pre-copulatory sexual selection relate to SSD across a broad range of animal taxa comprising up to 95 effect sizes from 59 species. We found that SSD based on length measurements was correlated with the sex difference in the opportunity for sexual selection but showed a weak and statistically non-significant relationship with the sex difference in the Bateman gradient. These findings suggest that pre-copulatory sexual selection plays a limited role for the evolution of SSD in a broad phylogenetic context.     

Banded karyotypes of mole rats (Spalax, Spalacidae, Rodentia) from Turkey: a comparative analysis

Chromosome banding (G-, C- and Ag-NOR) analysis was carried out on 27 specimens of Sphalax ehrenbergi from seven localities and two specimens of S. leucodon from one locality, all from Turkey. No chromosomal variation was detected in S. ehrenbergi populations from Elazig, Siverek, Diyarbakir and Birecik having the same diploid numbers (2n = 52) and morphology of chromosomes (NFa = 72). The karyotypes of mole rats from Tarsus and Gaziantep possessed the identical diploid number (2n = 56) but different numbers of autosomal arms: NFa = 68 in the Tarsus and NFa = 78 in the Gaziantep populations. Chromosomes of S. leucodon from Malaty (2n = 60, NFa = 74) differed distinctly in the C-banding pattern from all S. ehrenbergi cytotypes by the almost entire absence of heterochromatin in acrocentric autosomes and the presence of heterochromatin arms iin subtelocentric autosomes. Nucleolar organizing regions were found mainly on three pairs of chromosomes, but some differences in their localization were revealed. Comparison of G-banded chromosomes showed, that most chromosomes have a similar pattern. The types of chromosomal rearrangemetns were revealed due to the banding methods.     

Macroevolutionary patterns of bumblebee body size: detecting the interplay between natural and sexual selection

Bumblebees and other eusocial bees offer a unique opportunity to analyze the evolution of body size differences between sexes. The workers, being sterile females, are not subject to selection for reproductive function and thus provide a natural control for parsing the effects of selection on reproductive function (i.e., sexual and fecundity selection) from other natural selection. Using a phylogenetic comparative approach, we explored the allometric relationships among queens, males, and workers in 70 species of bumblebees (Bombus sp.). We found hyperallometry in thorax width for males relative to workers, indicating greater evolutionary divergence of body size in males than in sterile females. This is consistent with the hypothesis that selection for reproductive function, most probably sexual selection, has caused divergence in male size among species. The slope for males on workers was significantly steeper than that for queens on workers and the latter did not depart from isometry, providing further evidence of greater evolutionary divergence in male size than female size, and no evidence that reproductive selection has accelerated divergence of females. We did not detect significant hyperallometry when male size was regressed directly on queen size and our results thus add the genus Bombus to the increasing list of clades that have female-larger sexual size dimorphism and do not conform to Rensch's rule when analyzed according to standard methodology. Nevertheless, by using worker size as a common control, we were able to demonstrate that bumblee species do show the evolutionary pattern underlying Rensch's rule, that being correlated evolution of body size in males and females, but with greater evolutionary divergence in males.     

Pelvic dimorphism in relation to body size and body size dimorphism in humans

Many mammalian species display sexual dimorphism in the pelvis, where females possess larger dimensions of the obstetric (pelvic) canal than males. This is contrary to the general pattern of body size dimorphism, where males are larger than females. Pelvic dimorphism is often attributed to selection relating to parturition, or as a developmental consequence of secondary sexual differentiation (different allometric growth trajectories of each sex). Among anthropoid primates, species with higher body size dimorphism have higher pelvic dimorphism (in converse directions), which is consistent with an explanation of differential growth trajectories for pelvic dimorphism. This study investigates whether the pattern holds intraspecifically in humans by asking: Do human populations with high body size dimorphism also display high pelvic dimorphism? Previous research demonstrated that in some small-bodied populations, relative pelvic canal size can be larger than in large-bodied populations, while others have suggested that larger-bodied human populations display greater body size dimorphism. Eleven human skeletal samples (total N: male = 229, female = 208) were utilized, representing a range of body sizes and geographical regions. Skeletal measurements of the pelvis and femur were collected and indices of sexual dimorphism for the pelvis and femur were calculated for each sample [ln(M/F)]. Linear regression was used to examine the relationships between indices of pelvic and femoral size dimorphism, and between pelvic dimorphism and female femoral size. Contrary to expectations, the results suggest that pelvic dimorphism in humans is generally not correlated with body size dimorphism or female body size. These results indicate that divergent patterns of dimorphism exist for the pelvis and body size in humans. Implications for the evaluation of the evolution of pelvic dimorphism and rotational childbirth in Homo are considered.     

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

Karyotype (2fl) and allozymc 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; lour populations). We identified remarkable variation of diploid chromosome numbers in the S. leucodon superspecies: 2 n = 38. 40. 50, 54, 60 and 62; and in the S. ehrenbergi superspecies: 2 n = 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-5%= 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, 2 n , as good biological species. Karyotypic diversity may mark extensive ecological speciation. Nei's 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 biolir factors. Both In and H are significantly correlated with aridity stress (2 n /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 (allozymc) diversity and divergence in mole rat evolution, in both speciation and adaptation.     

Ribosomal DNA non-transcribed spacer polymorphism in subterranean mole rats: genetic differentiation,environmental correlates and phylogenetic relationships

Summary An analysis is presented of genetic differentiation in the non-transcribed spacers of ribosomal DNA (NTS rDNA). Diversity, environmental correlates and the phylogenetic relationships are examined within and between species of the actively speciating subterranean mole rat, superspeciesSpalax ehrenbergi (2n=52, 54, 58, 60) in Israel. This analysis is based on a previous study of the geographic distribution of restriction fragment length polymorphisms of NTS rDNA. Here we present results indicating that NTS rDNA diversity exists mostly (66%) within populations, while 20% is between populations within species, and 14% between species. Multivariate discriminant analysis succeeded in separating 10 of the 13 populations (77%) into their correct chromosomal species, on the basis of the combination of three NTS rDNA repetypes. The phylogenetic relationships suggest that the complex involves two pairs of closely related species (2n=52–54 and 2n=58–60). NTS rDNA diversity, as well as the decrease southward in frequency of repetype C, are correlated with climatic factors of humidity and temperature. These data are discussed in terms of the evolutionary forces of migration and selection which may cause NTS rDNA differentiation. Climatic selection appears to be the major differentiating factor of NTS rDNA.     

Spatiotemporal variation in selection on body size in the dung fly Sepsis cynipsea

Standardized measures of the strength of selection on a character allow quantitative comparisons across populations in time and space. Spatiotemporal variation in selection influences patterns of adaptation and the evolution of characters and must therefore be documented. For the dung-breeding fly Sepsis cynipsea, we document patterns of variation in sexual, fecundity and larval and adult viability selection on body size at several spatiotemporal scales: between-populations, over the season, over the day and between dung pats. Adult viability selection based on residual physiological survivorship in the laboratory was nil or weakly negative. In contrast, larval viability selection in two laboratory environments was weakly positive for males at low competition and females at high competition. Fecundity selection was positive and strong at all times and in all populations. Sexual selection reflecting pairing success was overall strongly positive (about three times stronger than fecundity selection), while selection reflecting male reproductive success via the clutch size of his mate (i.e. assortative mating) was essentially nil. Only sexual selection varied significantly at coarse (between populations and seasonally) but not at fine (within a day or between pats on a pasture) spatial and temporal scales. Quadratic and correlational selection differentials were low and inconsistent in all episodes except for fecundity selection, where there was some evidence that clutch size reaches an asymptote at large body sizes, implying weaker selection for large size as females get bigger. Implications of these results for the evolution of body size and body size dimorphism are discussed.     

Sexual size dimorphism in shorebirds, gulls, and alcids: the influence of sexual and natural selection

Abstract. Charadrii (shorebirds, gulls, and alcids) have an unusual diversity in their sexual size dimorphism, ranging from monomorphism to either male-biased or female-biased dimorphism. We use comparative analyses to investigate whether this variation relates to sexual selection through competition for mates or natural selection through different use of resources by males and females. As predicted by sexual selection theory, we found that in taxa with socially polygynous mating systems, males were relatively larger than females compared with less polygynous species. Furthermore, evolution toward socially polyandrous mating systems was correlated with decreases in relative male size. These patterns depend on the kinds of courtship displays performed by males. In taxa with acrobatic flight displays, males are relatively smaller than in taxa in which courtship involves simple flights or displays from the ground. This result remains significant when the relationship with mating system is controlled statistically, thereby explaining the enigma of why males are often smaller than females in socially monogamous species. We did not find evidence that evolutionary changes in sexual dimorphism relate to niche division on the breeding grounds. In particular, biparental species did not have greater dimorphism in bill lengths than uniparental species, contrary to the hypothesis that selection for ecological divergence on the breeding grounds has been important as a general explanation for patterns of bill dimorphism. Taken together, these results strongly suggest that sexual selection has had a major influence on sexual size dimorphism in Charadrii, whereas divergence in the use of feeding resources while breeding was not supported by our analyses.     

Sexual size and shape dimorphism and allometric scaling patterns in head traits in the New Zealand common gecko Woodworthia maculatus

Sexual dimorphism in shape and size is widespread across animal taxa and arises when natural or sexual selection operates differently on the sexes. Male and female common geckos (Woodworthia maculatus; formerly Hoplodactylus maculatus) in New Zealand do not appear to experience different viability selection pressure, nor do males appear to be under intense pre-copulatory sexual selection. It was therefore predicted that this species would be sexually monomorphic with regard to body size and the size and shape of the head. In line with the prediction, there was no sexual difference in head width, depth, or length or in lateral head shape. However, contrary to prediction, males had a larger body and lateral head size than females. This study suggests that males, at least on Maud Island, NZ, might be under stronger pre-copulatory sexual selection than previously recognized and thus have evolved larger heads (i.e. lateral head size) for use in male combat for females. Allometric scaling patterns do not differ between the sexes and suggest that head width and depth are under directional selection whereas lateral head size is under stabilizing selection. Diet ecology – an agent of natural selection common to both sexes – is likely largely responsible for the observed patterns of head size and shape and the lack of sexual dimorphism in them.     

Sexual selection versus alternative causes of sexual dimorphism in teiid lizards

Summary The presence and extent of sexual dimorphisms in body form (size and shape) of adult macroteiid lizards were investigated. Males were significantly larger than females in the temperate species, Cnemidophorus tigris, and in the tropical species, Ameiva ameiva and C. ocellifer. Young adult C. tigris males grew faster than young adult females within and between reproductive seasons. Adult males of all species had larger heads than adult females of the same body size; this difference increased with body size. Moreover, male C. tigris were heavier than females of the same snout-vent length. The causes and consequences of the sexual dimorphisms were also examined. The possible causes of body size are especially numerous, and distinguishing the relative influences of the various causal selection factors on body size is problematical. Nevertheless, observational field data were used to tentatively conclude that intrasexual selection was the cause of larger body size of C. tigris males relative to females because (1) larger males won in male aggressive interactions, (2) the winning males gained access to more females by repelling competitors and by female acceptance, (3) larger males consequently had higher reproductive success, and (4) other hypothetical causes of larger male size were unsupported.     

Sexual selection constrains the body mass of male but not female mice

Sexual size dimorphism results when female and male body size is influenced differently by natural and sexual selection. Typically, in polygynous species larger male body size is thought to be favored in competition for mates and constraints on maximal body size are due to countervailing natural selection on either sex; however, it has been postulated that sexual selection itself may result in stabilizing selection at an optimal mass. Here we test this hypothesis by retrospectively assessing the influence of body mass, one metric of body size, on the fitness of 113 wild‐derived house mice (Mus musculus) residing within ten replicate semi‐natural enclosures from previous studies conducted by our laboratory. Enclosures possess similar levels of sexual selection, but relaxed natural selection, relative to natural systems. Heavier females produced more offspring, while males of intermediate mass had the highest fitness. Female results suggest that some aspect of natural selection, absent from enclosures, acts to decrease their body mass, while the upper and lower boundaries of male mass are constrained by sexual selection.     

Sexual selection effects on the evolution of senescence

Although the basic theories concerning evolution of senescence have been generally accepted for a half-century, interpretation of this paradigm has been constrained by an over-reliance on mortality as both the cause and the measure of senescence. Consideration of both survival and fecundity as components of reproductive value, and integration of sexual selection theory with senescence theory allows reconciliation of long-standing, as well as recent, discrepancies between data and theory. This approach demonstrates that sexual selection on males in polygynous mating systems can have significant effects on the evolution of senescence that could overshadow the selection effects of mortality rates among such animals.     

Sexual selection: Another Darwinian process

Why was sexual selection so important to Darwin? And why was it de-emphasized by almost all of Darwin's followers until the second half of the 20th century? These two questions shed light on the complexity of the scientific tradition named “Darwinism”. Darwin's interest in sexual selection was almost as old as his discovery of the principle of natural selection. From the beginning, sexual selection was just another “natural means of selection”, although different from standard “natural selection” in its mechanism. But it took Darwin 30 years to fully develop his theory, from the early notebooks to the 1871 book The Descent of Man, and Selection in Relation to Sex. Although there is a remarkable continuity in his basic ideas about sexual selection, he emphasized increasingly the idea that sexual selection could oppose the action of natural selection and be non adaptive. In time, he also gave more weight to mate choice (especially female choice), giving explicit arguments in favor of psychological notions such as “choice” and “aesthetic sense”. But he also argued that there was no strict demarcation line between natural and sexual selection, a major difficulty of the theory from the beginning. Female choice was the main reason why Alfred Russel Wallace, the co-discoverer of the principle of natural selection, engaged in a major controversy with Darwin about sexual selection. Wallace was suspicious about sexual selection in general, trying to minimize it by all sorts of arguments. And he denied entirely the existence of female choice, because he thought that it was both unnecessary and an anthropomorphic notion. This had something to do with his spiritualist convictions, but also with his conception of natural selection as a sufficient principle for the evolutionary explanation of all biological phenomena (except for the origin of mind). This is why Wallace proposed to redefine Darwinism in a way that excluded Darwin's principle of sexual selection. The main result of the Darwin–Wallace controversy was that most Darwinian biologists avoided the subject of sexual selection until at least the 1950 s, Ronald Fisher being a major exception. This controversy still deserves attention from modern evolutionary biologists, because the modern approach inherits from both Darwin and Wallace. The modern approach tends to present sexual selection as a special aspect of the theory of natural selection, although it also recognizes the big difficulties resulting from the inevitable interaction between these two natural processes of selection. And contra Wallace, it considers mate choice as a major process that deserves a proper evolutionary treatment. The paper's conclusion explains why sexual selection can be taken as a test case for a proper assessment of “Darwinism” as a scientific tradition. Darwin's and Wallace's attitudes towards sexual selection reveal two different interpretations of the principle of natural selection: Wallace's had an environmentalist conception of natural selection, whereas Darwin was primarily sensitive to the element of competition involved in the intimate mechanism of any natural process of selection. Sexual selection, which can lack adaptive significance, reveals this exemplarily.