Correlation between variability and body size in vertebrates

An analysis of allozymic variation carried out in the main groups of vertebrate animals revealed a tendency towards the increased level of genetic polymorphism in the species of small animals compared to the large ones. This tendency was clearly followed in caudate amphibians, fishes, and mammals. The data are discussed in terms of the integration of monogenic and polygenic systems in the populations. It is hypothesized that this relationship between heterozygosity and body size confirms more general regularity consisting in highly statistically significant correlation between polygenic heterozygosity, maturation rate and life span. It is suggested that high rate of development in small animals resulting in early sexual maturation, can serve as a mechanism determining correlation between heterozygosity and body size at the species level. As a result, compared to large animals, small animals display higher rates of generation change, resulting in accelerated growth of population size and faster accumulation of genetic variability.     

RELATIONSHIPS BETWEEN GENETIC VARIABILITY AND LIFE-HISTORY FEATURES OF BONY FISHES

Correlations between genetic variation and life-history variables were obtained for 80 species of bony fishes as a means of testing the hypothesis that genetic variation is directly related to 1) opportunity for balancing selection, as indicated by fecundity, and 2) environmental variation, as indicated by capacity for population increase. Genetic data were taken from the literature, and data on longevity, age at maturity, egg size, body size, and lifetime fecundity were taken from the literature where available and were otherwise estimated from other variables. Average heterozygosity does not increase significantly with increasing fecundity. However, heterozygosity is significantly associated with short generation times, quick maturation, small maximum size, and small eggs. Thus, heterozygosity appears to increase on a demographic continuum toward maximum values in species that are most strongly selected for maximizing the intrinsic rate of increase. Such species are associated with less stable environments. Thus, the results indicate a predominate role for environmental variation in controlling genetic variation of bony fishes.     

FLUCTUATING ASYMMETRY IN CENTRAL AND MARGINAL POPULATIONS OF LYCHNIS VISCARIA IN RELATION TO GENETIC AND ENVIRONMENTAL FACTORS

Developmental instability in the form of increased fluctuating asymmetry can be caused by either genetic or environmental stress. Because extinctions can be attributed broadly to these factors, fluctuating asymmetry may provide a sensitive tool for detecting such stresses. We studied the level of fluctuating asymmetry of flowers of a perennial outcrossing plant species, Lychnis viscaria, both in natural and common-garden populations. The degree of flower asymmetry was higher in small, isolated, and marginal populations of the species range. These marginal populations also were the most homozygous. In the core area of the species' range, flowers were more symmetrical The level of asymmetry was correlated with both population size and heterozygosity. However, a partial correlation analysis revealed that when the impact of population size was controlled for, there was a negative relationship between fluctuating asymmetry and heterozygosity, whereas when controlling for heterozygosity, no relationship between population size and fluctuating asymmetry was found. This indicates that genetic consequences of small population size probably underlie the relationship between the level of asymmetry and population size. Results from a transplantation experiment showed that individuals subjected to a higher environmental stress had an increased level of asymmetry compared to control plants. In the common-garden conditions the level of fluctuating asymmetry did not differ between the central and marginal populations. This suggests that presumably both genetic and environmental factors affected to the higher level of asymmetry among marginal populations compared to central ones. In all we conclude that even though fluctuating asymmetry seems to be a sensitive tool for detecting stresses, results from studies focusing on only one factor should be interpreted with caution.     

Environment-dependent genetic correlations between development time and body mass in a scorpionfly

Development time and body mass at maturation are two important fitness traits fundamental for our understanding of life history theory. Generally, fast development is associated with small adult body mass, as it will take longer to grow large. However, the strength of this trade-off may depend on average food availability, as the potential benefit of long development will depend on the rate of food intake. Here, I report results of a food manipulation experiment during larval development of the scorpionfly Panorpa cognata (Insecta, Mecoptera). Development time showed considerable genetic variation, yet food level had no influence and there was a strong genetic correlation in development time across environments. As expected, larval and adult body weight was significantly affected by food availability. Furthermore, body mass was influenced by a highly significant genotype-by-environment interaction. The reaction norm for body mass in response to food treatment was much stronger in families with long development time compared with rapidly developing genotypes. This effect was accompanied by a shift in the genetic correlation between development time and body size when comparing the two food levels. Specifically, the genetic correlation between body mass and development time changed from being positive at high food levels to a negative genetic correlation at low food levels. These results are consistent with other empirical findings demonstrating a similar shift in genetic correlations between body mass and development time when comparing favourable and unfavourable environmental conditions.     

Cytochrome b phylogeny and the taxonomy of great apes and mammals

In the Linnaean system of classification, the generic status of a species is part of its binomial name, and it is therefore important that the classification at the level of genus is consistent at least in related groups of organisms. Using maximum-likelihood phylogenetic trees constructed from a large number of complete or nearly complete mammalian cytochrome b sequences, I show that the distributions of intrageneric and intergeneric distances derived from these trees are clearly separated, which allows the limits for a more rational generic classification of mammals to be established. The analysis of genetic distances among hominids in this context provides strong support for the inclusion of humans and chimpanzees in the same genus. It is also of interest to decipher the main reasons for the possible biases in the mammalian classification. I found by correlation analysis that the classification of mammals of large body size tends to be oversplit, whereas that of small mammals has an excess of lumping, which may be a manifestation of the larger difficulty in finding diagnostic characters in the classification of small animals. In addition, and contrary to some previous observations, there is no correlation between body size and rate of cytochrome b evolution in mammals, which excludes the difference in evolutionary rates as the cause of the observed body size taxonomic bias.     

Trade‐offs between growth and reproduction: an analysis of the quantitative genetic evidence

The assumption of a trade‐off between development time and fecundity, resulting from a positive correlation between body size and fecundity and between body size and development time, is a common feature of life history models. The present paper examines the evidence for such a trade‐off as indicated by genetic correlations between traits. The genetic covariances between traits are derived using a model in which maturation occurs when the organism achieves a genetically variable size threshold, and fecundity is an allometric function of body size with one genetically variable parameter (excluding body size itself). This model predicts that the heritabilities of the life history traits (growth rate, development time, fecundity) will not necessarily be less than the heritability of adult size (i.e. morphological traits). It is shown that if growth rate is genetically correlated with adult size then it is not possible, in general, to predict the sign of the genetic correlation between development time and fecundity. For particular cases the signs of the covariances between traits can be predicted. These predictions are tested using data drawn from the literature.     

Estimation of average heterozygosity and genetic distance from a small number of individuals

The magnitudes of the systematic biases involved in sample heterozygosity and sample genetic distances are evaluated, and formulae for obtaining unbiased estimates of average heterozygosity and genetic distance are developed. It is also shown that the number of individuals to be used for estimating average heterozygosity can be very small if a large number of loci are studied and the average heterozygosity is low. The number of individuals to be used for estimating genetic distance can also be very small if the genetic distance is large and the average heterozygosity of the two species compared is low.     

Efficiency of selection, as measured by single nucleotide polymorphism variation, is dependent on inbreeding rate in Drosophila melanogaster

It is often hypothesized that slow inbreeding causes less inbreeding depression than fast inbreeding at the same absolute level of inbreeding. Possible explanations for this phenomenon include the more efficient purging of deleterious alleles and more efficient selection for heterozygote individuals during slow, when compared with fast, inbreeding. We studied the impact of inbreeding rate on the loss of heterozygosity and on morphological traits in Drosophila melanogaster. We analysed five noninbred control lines, 10 fast inbred lines and 10 slow inbred lines; the inbred lines all had an expected inbreeding coefficient of approximately 0.25. Forty single nucleotide polymorphisms in DNA coding regions were genotyped, and we measured the size and shape of wings and counted the number of sternopleural bristles on the genotyped individuals. We found a significantly higher level of genetic variation in the slow inbred lines than in the fast inbred lines. This higher genetic variation was resulting from a large contribution from a few loci and a smaller effect from several loci. We attributed the increased heterozygosity in the slow inbred lines to the favouring of heterozygous individuals over homozygous individuals by natural selection, either by associative over‐dominance or balancing selection, or a combination of both. Furthermore, we found a significant polynomial correlation between genetic variance and wing size and shape in the fast inbred lines. This was caused by a greater number of homozygous individuals among the fast inbred lines with small, narrow wings, which indicated inbreeding depression. Our results demonstrated that the same amount of inbreeding can have different effects on genetic variance depending on the inbreeding rate, with slow inbreeding leading to higher genetic variance than fast inbreeding. These results increase our understanding of the genetic basis of the common observation that slow inbred lines express less inbreeding depression than fast inbred lines. In addition, this has more general implications for the importance of selection in maintaining genetic variation.     

Variation of loci encoding homologous enzymes in an evolutionary series of vertebrates

A study of variability of 11 allozyme loci (sAat, G3pdh, Gpi, sIdh, Ldh-A, Ldh-B, sMdh, sMe, sSod, Pgdh, and Sdh) in the evolutionary series of vertebrates from Cyclostomat to Mammalia revealed that (1) in vertebrates, these loci encoding multimeric enzymes are characterized by different heterozygosity levels, the extremes of which (represented by loci Ldh-A and Pgdh) differ from each other more than by a factor of 4; (2) classes of vertebrates markedly differed from one another in genetic variation; lower Tetrapoda are characterized by the highest level of genetic polymorphism, the classes representing the margins of the phyletic line-primitive (Cyclostomata and Chondrchthyes) and advanced (Aves and Mammalia)--have minimum heterozygosity levels, whereas Osteichthyes are characterized by intermediate heterozygosity level; (3) in the evolutionary series of vertebrates, heterozygosity varies rather independently in the groups of loci characterized by low, medium, and high variability. These patterns are explained in the context of intraorganismic factors: integration of mono- and polygenic traits (primarily, body size and ontogeny rate) and evolutionary specialization.     

Heritable body size mediates apparent life-history trade-offs in a simultaneous hermaphrodite

Physiological trade-offs between life-history traits can constrain natural selection and maintain genetic variation in the face of selection, thereby shaping evolutionary trajectories. This study examines physiological trade-offs in simultaneously hermaphroditic banana slugs, Ariolimax dolichophallus. These slugs have high heritable variation in body size, which strongly predicts the number of clutches laid, hatching success and progeny growth rate. These fitness components were associated, but only when examined in correlation with body size. Body size mediated these apparent trade-offs in a continuum where small animals produced rapidly growing progeny, intermediate-sized animals laid many clutches and large animals had high hatching success. This study uses a novel statistical method in which the components of fitness are analysed in a mancova and related to a common covariate, body size, which has high heritability. The mancova reveals physiological trade-offs among the components of fitness that were previously masked by high variation in body size.     

Timing of maturation and the mating system of the spider,Stegodyphus lineatus (Eresidae): how important is body size?

Selection on life history traits such as the timing of maturation and the size at maturity strongly depends on the mating system. In spiders, the mating system hypothesized to Be determined by spermathecal morphology and the related sperm precedence pattern. In a natural population of the eresid spider Stegodyphus lineatus , predictions concerning the timing of maturation, male mating behaviour and success were tested. Eresid spiders are supposed to show protandry, prematuration mate guarding and strong male-male competition resulting in selection for large body size and early maturation. In contrast to these predictions, male and female maturation overlapped largely. Males did not guard premature females nor was there evidence for male-male competition. Among mating pairs, male did not relate to female size, nor to duration of cohabitation. Evidence for an advantage of first over second or large over small males is weak. In males, body size at maturity and the time of maturation were negatively correlated although a trade off between timing of maturation and the body size reached by then should result in a positive correlation. Possible causes are discussed.     

Generic species richness and body mass in North American mammals: Support for the inverse relationship of body size and speciation rate

Generic species richness, the number of species per genus, is examined as a function of mean generic body mass for extant North American mammals. Species richness decreases as an inverse power function with increased mass, and the Spearman rank correlation coefficient of the logio transformed data is significant (r_s= ‐0.37). When the data are partitioned by trophic level, the relationship is not statistically significant for carnivores but strengthens for herbivores (r_s= ‐0.46). This interesting but incidental effect is due to the negligible number of diminutive and excessively large carnivores, which is in turn determined by foraging strategies. Alternate hypotheses for the “right‐skewed”; size distribution of modern North American mammals, such as disproportionate extinction of large species, differential species longevity, and a geographical scaling function, are rejected in favor of the proposition that elevated levels of speciation are restricted to animals of small body mass, as originally proposed by Gould and Eldredge (1977). This phenomenon is explained as a function of habitat restriction and particularly in herbivores, limited home range size. Aquatic mammals, regardless of body size, speciate rarely. Cope's Rule, the tendency of many animal groups to evolve towards large size, is understood as a probabilistic statement reflecting the phylogenetic tendencies of a disproportionately high number of small species alive at any given point in time.     

Small body size increases the regional differentiation of populations of tropical mantellid frogs (Anura: Mantellidae)

The processes affecting species diversification may also exert an influence on patterns of genetic variability within species. We evaluated the contributions of five variables potentially influencing clade diversification (body size, reproductive mode, range size, microhabitat and skin texture) on mtDNA divergence and polymorphism among populations of 40 species of frogs (Mantellidae) from two rainforest communities in Madagascar. We report an inverse association between body size and nucleotide divergence between populations but find no influence of other variables on genetic variation. Body size explained ca. 11% of the variation in nucleotide divergence between populations and was coupled with high F_ST levels and an absence of haplotype sharing in small‐bodied and medium‐sized frogs. Low dispersal ability is likely the proximate mechanism producing higher population differentiation in small mantellids. The lack of genetic cohesion among populations establishes regional genetic fragmentation which in turn has the potential to accelerate rates of allopatric speciation in small frogs relative to large species. However, there is little evidence of increased speciation rates in these or other small‐bodied organisms. We reconcile these contradictory observations by suggesting that lower dispersal ability also curbs colonization of new areas, decelerating diversification in weak dispersers. Our results imply that the intermediate dispersal model also applies to amphibians and may explain inconsistent previous results on the correlation of body size and speciation rate.     

Body size and the daily rhythm of body temperature in dogs

Practically every physiological variable exhibits daily rhythmicity. The daily rhythm of body temperature, like that of many other variables, is often weak in newborns and gains strength as the animals grow. Because of the natural association between physiological maturation and gain in body size, these two processes are naturally confounded. To differentiate between the effects of maturation and the effects of body growth, we took advantage of the large variation in body size that exists among different breeds of the domestic dog. We compared the body temperature rhythms of developing puppies of different dog breeds. Puppies of none of the breeds exhibited statistically significant daily rhythmicity for several days after birth. Regardless of breed or sex, rhythmicity matured over several weeks and attained a stable level by 6 weeks after birth. Body size did not seem to be an important element in the development of rhythmicity because the development was similar in three breeds that differed greatly in body size (Basset Hound, Boxer, and Neapolitan Mastiff). On the other hand, the difference in body size associated with the different breeds had a strong impact on the absolute level of body temperature regardless of age: we found a strong inverse correlation between temperature and body size among the puppies and dams of the three breeds and among 115 adult dogs from 19 different breeds ranging from 2-kg Yorkshire Terriers to 80-kg Great Danes.     

Intestinal length of three California pinniped species

Forty-eight intestinal tracts, extracted from both sexes of California sea lions, Harbour seals and Northern elephant seals, were measured. The majority of intestinal tracts were removed from stranded animals that died from various causes. The sea lions and elephant seals, approximately equal in size, were larger than the Harbour seals. All species possess a small intestine which is significantly longer than even the entire gastrointestinal tract of herbivores of comparable size. Elephant seal small intestines, averaging approximately 25 times the seal's body length, were considerably longer than the small intestines of either sea lions (averaged more than 18 times the body length) or Harbour seals (averaged nearly 16 times the body length). However, the large intestines of elephant seals were shorter than either of the other two species. Among the sea lions and Harbour seals the large intestines were approximately equal in length. Sea lions and Harbour seals also showed a close correlation between standard length and total intestinal length. Among elephant seals these two parameters showed greater variability. The functional significance of the extremely long small intestine remains unclear. Certainly, the large body mass and high energy requirements of these animals has contributed to the development of a long intestinal tract. It also appears likely that diet and the high motility rate of digesta influenced the intestinal development. Comparatively, the significantly shorter large intestine of elephant seals probably relates to this species' remarkable capabilities in water conservation and metabolic water retention.     

The heterozygosity for the biochemical and immunological markers of genes and the variability of morphophysiological traits in man

The relationship between heterozygosity of 9 biochemical and 5 blood group loci and variability of body length and age of menarche were studied in 467 women and 336 men from Moscow population. High and low levels of individual heterozygosity were shown in men to be associated with the maximal values of the coefficient of variation (CV) of body length, while in women strong positive correlation between the CV of body length and individual heterozygosity was demonstrated. The highest level of heterozygosity was revealed in medium-height men and low-height women. Highly heterozygous women were characterized either by early or by late age of menarche; early onset of menarche causes growth retardation. Positive correlation between the CV of body length and heterozygosity in women is due to the accumulation of low-height individuals having early age of menarche. The results are discussed in terms of Lerner's concept of genetic homeostasis. It is concluded that an average level of heterozygosity is optimal for a population.     

Is genomic diversity a useful proxy for census population size? Evidence from a species‐rich community of desert lizards

Species abundance data are critical for testing ecological theory, but obtaining accurate empirical estimates for many taxa is challenging. Proxies for species abundance can help researchers circumvent time and cost constraints that are prohibitive for long‐term sampling. Under simple demographic models, genetic diversity is expected to correlate with census size, such that genome‐wide heterozygosity may provide a surrogate measure of species abundance. We tested whether nucleotide diversity is correlated with long‐term estimates of abundance, occupancy and degree of ecological specialization in a diverse lizard community from arid Australia. Using targeted sequence capture, we obtained estimates of genomic diversity from 30 species of lizards, recovering an average of 5,066 loci covering 3.6 Mb of DNA sequence per individual. We compared measures of individual heterozygosity to a metric of habitat specialization to investigate whether ecological preference exerts a measurable effect on genetic diversity. We find that heterozygosity is significantly correlated with species abundance and occupancy, but not habitat specialization. Demonstrating the power of genomic sampling, the correlation between heterozygosity and abundance/occupancy emerged from considering just one or two individuals per species. However, genetic diversity does no better at predicting abundance than a single day of traditional sampling in this community. We conclude that genetic diversity is a useful proxy for regional‐scale species abundance and occupancy, but a large amount of unexplained variation in heterozygosity suggests additional constraints or a failure of ecological sampling to adequately capture variation in true population size.     

Changes in reproductive strategy in the ruffe during a period of establishment in a new habitat

The pattern of maturation, body size and fecundity was examined in a population of ruffe ( Gymnocephalus cernuus L.) three times during a period of rapid growth, and eventual stabilization, following its introduction to a new habitat. When the ruffe were less common, maturing ruffe were relatively large and immature ruffe relatively small, compared with when the ruffe were abundant. Intermediate ruffe population size showed a maturation pattern intermediate between these two extremes. It is suggested that this pattern of maturation is a response of the ruffe population to changing growth opportunity induced by changing intraspecific competition. This fluctuating maturation pattern is interpreted in terms of a threshold-dependent maturation trigger, operating on the rate of accumulation of energy and a trade-off between somatic growth and gonad development. When the ruffe population was large, high intraspecific competition resulted in low opportunity for growth; only fish with the highest rate of food acquisition were able to mature in a given year–the investment in gonadal tissue reducing somatic growth. When the ruffe population was low, the high rate of energy acquisition in the population resulted in the triggering of maturation, even at small size, only the very smallest fish remaining immature. High growth opportunity allowed maturing fish to develop gonad and maintain somatic growth. The pattern of size related fecundity also changed over the three periods. When growth opportunity was low, size related fecundity was greater than when opportunity for growth was high. This suggests that maturing females faced with poor growth conditions compensated by increasing egg number for a given body size either by decreasing egg size or by increasing total investment in ovarian tissue.     

Predation, group size and mortality in a cooperative mongoose, Suricata suricatta

1. In social mammals where group members cooperate to detect predators and raise young, members of small groups commonly show higher mortality or lower breeding success than members of large ones. It is generally assumed that this is because large group size allows individuals to detect or repel predators more effectively but other benefits of group size may also be involved, including reduced costs of raising young and more effective competition for resources with neighbouring groups.
2. To investigate the extent to which predation rate affects survival, we compared mortality rates in two populations of suricates ( Suricata suricatta ), one living in an area of high predator density (Kalahari Gemsbok Park) and one living in an area of relatively low predator density (neighbouring ranchland). Most aspects of feeding ecology and growth (including time spent feeding, daily weight gain, growth, adult body weight, breeding frequency and neonatal mortality) were similar in the two populations. In contrast, mortality of animals over 3 months old was 1·7 times higher in the Park than on ranchland.
3. Mortality of juveniles between emergence from the natal burrow and 6 months of age was higher in small groups than large ones in the Park but significantly lower in small groups than large ones on ranchland. Adult mortality declined in larger groups in both areas.
4. The tendency for survival to be low in small groups had far-reaching consequences for the risk of group extinction. During a year of low rainfall in the Park, all groups of less than nine animals became extinct and population density declined to around a third of its initial level. We argue that high group extinction rates are to be expected in species where survival declines in small groups and mortality rates are high.     

Inverse correlation of population similarity and introduction date for invasive ascidians

The genomes of many marine invertebrates, including the purple sea urchin and the solitary ascidians Ciona intestinalis and Ciona savignyi, show exceptionally high levels of heterozygosity, implying that these populations are highly polymorphic. Analysis of the C. savignyi genome found little evidence to support an elevated mutation rate, but rather points to a large population size contributing to the polymorphism level. In the present study, the relative genetic polymorphism levels in sampled populations of ten different ascidian species were determined using a similarity index generated by AFLP analysis. The goal was to determine the range of polymorphism within the populations of different species, and to uncover factors that may contribute to the high level of polymorphism. We observe that, surprisingly, the levels of polymorphism within these species show a negative correlation with the reported age of invasive populations, and that closely related species show substantially different levels of genetic polymorphism. These findings show exceptions to the assumptions that invasive species start with a low level of genetic polymorphism that increases over time and that closely related species have similar levels of genetic polymorphism.