Allometry of the baculum and sexual size dimorphism in American martens and fishers (Mammalia: Mustelidae)

Genitalia are among the most variable of morphological traits, and recent research suggests that this variability may be the result of sexual selection. For example, large bacula may undergo post‐copulatory selection by females as a signal of male size and age. This should lead to positive allometry in baculum size. In addition to hyperallometry, sexually selected traits that undergo strong directional selection should exhibit high phenotypic variation. Nonetheless, in species in which pre‐copulatory selection predominates over post‐copulatory selection (such as those with male‐biased sexual size dimorphism), baculum allometry may be isometric or exhibit negative allometry. We tested this hypothesis using data collected from two highly dimorphic species of the Mustelidae, the American marten (Martes americana) and the fisher (Martes pennanti). Allometric relationships were weak, with only 4.5–10.1% of the variation in baculum length explained by body length. Because of this weak relationship, there was a large discrepancy in slope estimates derived from ordinary least squares and reduced major axis regression models. We conclude that stabilizing selection rather than sexual selection is the evolutionary force shaping variation in baculum length because allometric slopes were less than one (using the ordinary least squares regression model), a very low proportion of variance in baculum length was explained by body length, and there was low phenotypic variability in baculum length relative to other traits. We hypothesize that this pattern occurs because post‐copulatory selection plays a smaller role than pre‐copulatory selection (manifested as male‐biased sexual size dimorphism). We suggest a broader analysis of baculum allometry and sexual size dimorphism in the Mustelidae, and other taxonomic groups, coupled with a comparative analysis and with phylogenetic contrasts to test our hypothesis. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 955–963.     

Effects of sample size and intraspecific variation in phylogenetic comparative studies: a meta‐analytic review

Comparative analyses aim to explain interspecific variation in phenotype among taxa. In this context, phylogenetic approaches are generally applied to control for similarity due to common descent, because such phylogenetic relationships can produce spurious similarity in phenotypes (known as phylogenetic inertia or bias). On the other hand, these analyses largely ignore potential biases due to within‐species variation. Phylogenetic comparative studies inherently assume that species‐specific means from intraspecific samples of modest sample size are biologically meaningful. However, within‐species variation is often significant, because measurement errors, within‐ and between‐individual variation, seasonal fluctuations, and differences among populations can all reduce the repeatability of a trait. Although simulations revealed that low repeatability can increase the type I error in a phylogenetic study, researchers only exercise great care in accounting for similarity in phenotype due to common phylogenetic descent, while problems posed by intraspecific variation are usually neglected. A meta‐analysis of 194 comparative analyses all adjusting for similarity due to common phylogenetic descent revealed that only a few studies reported intraspecific repeatabilities, and hardly any considered or partially dealt with errors arising from intraspecific variation. This is intriguing, because the meta‐analytic data suggest that the effect of heterogeneous sampling can be as important as phylogenetic bias, and thus they should be equally controlled in comparative studies. We provide recommendations about how to handle such effects of heterogeneous sampling.     

Sexual selection, sexual size dimorphism and Rensch's rule in Odonata

Odonata (dragonflies and damselflies) exhibit a range of sexual size dimorphism (SSD) that includes species with male-biased (males > females) or female-biased SSD (males < females) and species exhibiting nonterritorial or territorial mating strategies. Here, we use phylogenetic comparative analyses to investigate the influence of sexual selection on SSD in both suborders: dragonflies (Anisoptera) and damselflies (Zygoptera). First, we show that damselflies have male-biased SSD, and exhibit an allometric relationship between body size and SSD, that is consistent with Rensch's rule. Second, SSD of dragonflies is not different from unit, and this suborder does not exhibit Rensch's rule. Third, we test the influence of sexual selection on SSD using proxy variables of territorial mating strategy and male agility. Using generalized least squares to account for phylogenetic relationships between species, we show that male-biased SSD increases with territoriality in damselflies, but not in dragonflies. Finally, we show that nonagile territorial odonates exhibit male-biased SSD, whereas male agility is not related to SSD in nonterritorial odonates. These results suggest that sexual selection acting on male sizes influences SSD in Odonata. Taken together, our results, along with avian studies (bustards and shorebirds), suggest that male agility influences SSD, although this influence is modulated by territorial mating strategy and thus the likely advantage of being large. Other evolutionary processes, such as fecundity selection and viability selection, however, need further investigation.     

Sexual selection explains Rensch's rule of allometry for sexual size dimorphism

In 1950, Rensch first described that in groups of related species, sexual size dimorphism is more pronounced in larger species. This widespread and fundamental allometric relationship is now commonly referred to as 'Rensch's rule'. However, despite numerous recent studies, we still do not have a general explanation for this allometry. Here we report that patterns of allometry in over 5300 bird species demonstrate that Rensch's rule is driven by a correlated evolutionary change in females to directional sexual selection on males. First, in detailed multivariate analysis, the strength of sexual selection was, by far, the strongest predictor of allometry. This was found to be the case even after controlling for numerous potential confounding factors, such as overall size, degree of ornamentation, phylogenetic history and the range and degree of size dimorphism. Second, in groups where sexual selection is stronger in females, allometry consistently goes in the opposite direction to Rensch's rule. Taken together, these results provide the first clear solution to the long-standing evolutionary problem of allometry for sexual size dimorphism: sexual selection causes size dimorphism to correlate with species size.     

Rensch's rule, Bergmann's effect and adult sexual dimorphism in wild monogamous owl monkeys (Aotus azarai) of Argentina

Some monogamous primates are characterized by biparental care, territoriality, and a reduced level of physical dimorphism. In others, the relationship between those behavioral patterns and dimorphism is less clear. I tested Bergmann's and Rensch's rules using Aotus spp. body mass data and I characterized the extent of sexual dimorphism in body mass, dental and physical measurements in a socially monogamous owl monkey population (n = 91 adults) from the Argentinean Gran Chaco. A. azarai azarai from the Argentinean Chaco is larger than the more tropical owl monkey species (r = 0.7, N = 6 species), but there is no apparent increase in sexual dimorphism with increased body mass. The body masses of adult male and female A. a. azarai were remarkably similar (Mean = 1.26 kg); there were no marked sex differences in most skeletal measurements, but males had higher and wider upper and lower canines than did females. Body mass and neck circumference were positively and strongly related (r = 0.533, n = 52), and the body mass of adults was not a reliable indicator of their age (r = 0.03, n = 10). The data illustrate the complexities inherent in examining and summarizing within population variation in skeletal and nonskeletal measurements and contribute to a better understanding of the relationships between monogamous behavioral patterns and sexual dimorphism.     

Intraspecific variation in body size and sexual size dimorphism,and a test of Rensch's rule in bats

The magnitude and direction of sexual size dimorphism (SSD) may vary considerably within and among taxa, and the primary causes of such variation have not been thoroughly elucidated. For example, the effect of abiotic factors is frequently attributed to explain intra‐ and interspecific variation in SSD. Rensch's rule, which states that males vary more in size than females when body size increases, has rarely been tested in bats. Therefore, whether bats follow Rensch's rule remains unclear, particularly when females are larger than males. We investigated whether four bat species presented SSD, as well as whether their body sizes varied within each sex across localities, testing the hypothesis that intraspecific SSD varies substantially depending of sampling localities. We finally examined whether bats followed Rensch's rule by simultaneously using intraspecific and interspecific approaches. Although SSD was not observed for most bat species within each locality, the females of three of the four captured species exhibited differences in body size between particular localities. Usually the females varied more in size than did males across localities, mostly exhibiting a female‐biased SSD. Significant differences in SSD were observed (i.e. mean values of the sexual dimorphism index), even though Rensch's rule was not followed.     

Brains and bravery: Little evidence of a relationship between brain size and flightiness in shorebirds

The ability of birds to perceive, assess and appropriately respond to the presence of relatively novel threats is important to their survival. We hypothesized that the cognitive capacity of birds will influence their ability for accurate response to novelty. We used brain volume as a surrogate for cognitive capacity and postulated that larger brained birds would moderate their responses when presented with a benign, frequently occurring stimulus, such as a person, because they would habituate more readily. We conducted phylogenetic generalized least square regression to investigate the relationship between brain volume and flight initiation distance (FID; the distance to which a bird can be approached before initiating escape behaviour), while controlling for confounding factors including body size (body mass and wing length) and migration status. We compared seven different models using combinations of these parameters using Akaike's information criterion to determine the best approximating model(s) explaining FID. The two best‐supported models included only wing length and only body mass with Akaike weights of 0.396 and 0.311 respectively. No model including brain volume had an Akaike weight greater than 0.083 and brain volume was poorly correlated with FID in models after controlling for body mass. Thus, brain volume does not appear to strongly relate to bravery among these shorebirds.     

Pheromone production, male abundance, body size, and the evolution of elaborate antennae in moths

The males of some species of moths possess elaborate feathery antennae. It is widely assumed that these striking morphological features have evolved through selection for males with greater sensitivity to the female sex pheromone, which is typically released in minute quantities. Accordingly, females of species in which males have elaborate (i.e., pectinate, bipectinate, or quadripectinate) antennae should produce the smallest quantities of pheromone. Alternatively, antennal morphology may be associated with the chemical properties of the pheromone components, with elaborate antennae being associated with pheromones that diffuse more quickly (i.e., have lower molecular weights). Finally, antennal morphology may reflect population structure, with low population abundance selecting for higher sensitivity and hence more elaborate antennae. We conducted a phylogenetic comparative analysis to test these explanations using pheromone chemical data and trapping data for 152 moth species. Elaborate antennae are associated with larger body size (longer forewing length), which suggests a biological cost that smaller moth species cannot bear. Body size is also positively correlated with pheromone titre and negatively correlated with population abundance (estimated by male abundance). Removing the effects of body size revealed no association between the shape of antennae and either pheromone titre, male abundance, or mean molecular weight of the pheromone components. However, among species with elaborate antennae, longer antennae were typically associated with lower male abundances and pheromone compounds with lower molecular weight, suggesting that male distribution and a more rapidly diffusing female sex pheromone may influence the size but not the general shape of male antennae.     

Sampling effort, regression method, and the shape and slope of size–abundance relations

1. Despite a substantial body of work there remains much disagreement about the form of the relationship between organism abundance and body size. In an attempt at resolving these disagreements the shape and slope of samples from simulated and real abundance–mass distributions were assessed by ordinary least squares regression (OLS) and the reduced major axis method (RMA).
2. It is suggested that the data gathered by ecologists to assess these relationships are usually truncated in respect of density. Under these conditions RMA gives slope estimates which are consistently closer to the true slopes than OLS regression.
3. The triangular relationships reported by some workers are found over smaller mass and abundance ranges than linear relations. Scatter in slope estimates is much greater and positive slopes more common at small sample sizes and sample ranges. These results support the notion that inadequate and truncated sampling is responsible for much of the disagreement reported in the literature.
4. The results strongly support the notion that density declines with increasing body mass in a broad, linear band with a slope around −1. However there is some evidence to suggest that this overall relation results from a series of component relations with slopes which differ from the overall slope.     

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.     

Female-biased sexual size dimorphism in tinamous: a comparative test fails to support Rensch's rule

Rensch's rule states that degree of sexual dimorphism increases with body size in species with larger males, and decreases with body size in those with larger females. To test this rule, we assessed the pattern of sexual size dimorphism in tinamous using a comparative analysis of independent contrasts. Tinamous are a monophyletic group of primitive birds comprising at least 47 ground dwelling species with prominent or exclusive paternal care of eggs and offspring. Although the size of females exceeded that of males in most considered species, we found an isometric relationship between males and females, instead of the negative allometric one predicted by Rensch's rule. Previous studies in Strigiformes and Falconiformes found positive allometric and isometric relationships respectively, and, considering these findings with our results, we conclude that Rensch's rule is not supported by birds with exclusively female-biased sexual dimorphism in size.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 80 , 519–527     

Sexual size dimorphism in parasitic oxyurid nematodes

As in many invertebrates, female oxyurids are larger than male. Sexual size dimorphism (SSD) of oxyurid nematodes (the hosts of which are both invertebrate and vertebrate), is investigated regarding body size of both host and parasite. SSD of parasites appeared to be weakly, but not significandy, correlated with invertebrate and vertebrate host body size. However, this study reveals a different pattern for SSD with respect to either type of host. SSD does not increase in tandem with body size in vertebrate parasites either at the level of species or genus. SSD is much more pronounced in Syphaciidae than in Heteroxynematidae, two families of vertebrate parasites exhibiting different modes of transmission (members of the Syphaciidae are transmitted through perianal contamination). SSD is investigated in one monophyletic group of parasites of primates, for which a phylogeny is known. Independent comparisons method is used and we find that the body size of female parasite is strongly correlated with that of the male. The hypoallometry (slope<1) of the relationship suggests that the SSD is not linked to an increase of parasite body size. Moreover, there is no influence of host body size on parasite SSD. The pattern in parasites of invertebrates is different. First, SSD has been found to increase with parasite body size in two groups of invertebrate parasites: the oxyurids of Dictyoptera and Coleoptera. Second, female body size of invertebrate parasites is not correlated with male body size either at genus or species level. Finally, the evolution of SSD is discussed in relation to the demographic patterns of invertebrate parasites and the haplodiploid mode of reproduction of these parasitic nematodes.     

PHYLOGENETICALLY INFORMED ANALYSIS OF THE ALLOMETRY OF MAMMALIAN BASAL METABOLIC RATE SUPPORTS NEITHER GEOMETRIC NOR QUARTER-POWER SCALING

The form of the relationship between the basal metabolic rate (BMR) and body mass (M) of mammals has been at issue for almost seven decades, with debate focusing on the value of the scaling exponent ( b , where BMR ∝ M^b ) and the relative merits of b = 0.67 (geometric scaling) and b = 0.75 (quarter-power scaling). However, most analyses are not phylogenetically informed (PI) and therefore fail to account for the shared evolutionary history of the species they consider. Here, we reanalyze the most rigorously selected and comprehensive mammalian BMR dataset presently available, and investigate the effects of data selection and phylogenetic method (phylogenetic generalized least squares and independent contrasts) on estimation of the scaling exponent relating mammalian BMR to M. Contrary to the results of a non-PI analysis of these data, which found an exponent of 0.67–0.69, we find that most of the PI scaling exponents are significantly different from both 0.67 and 0.75. Similarly, the scaling exponents differ between lineages, and these exponents are also often different from 0.67 or 0.75. Thus, we conclude that no single value of b adequately characterizes the allometric relationship between body mass and BMR.     

Sexual size dimorphism in anadromous brown trout Salmo trutta

Anadromous trout Salmo trutta exhibits sexual size dimorphism (S_SD); females were larger than males in populations where male mean total length (L_T) at maturity was below 49 cm and females were smaller than males when mean male L_T was above 49 cm, the slope of the regression of female on male L_T was 0·59. In streams with mean annual discharge below 41 m³ s^?1, flow added significantly to a model with S_SD as the dependent variable and male mean L_T at maturity as the first predictor variable. There was a slight increase in S_SD with increasing latitude, which may result from an increase in male size with increasing latitude.     

Patterns of sexual size dimorphism in Chelonia

Macroevolutionary patterns of sexual size dimorphism (SSD) indicate how sexual selection, natural selection, and genetic and developmental constraints mold sex differences in body size. One putative pattern, known as Rensch's rule, posits that, among species with female‐larger SSD, the relative degree of SSD declines with species' body size, whereas, among male‐larger SSD species, relative SSD increases with size. Using a dataset of 196 chelonian species from all fourteen families, we investigated the correlation in body size evolution between male and female Chelonia and the validity of Rensch's rule for the taxon and within its major clades. We conclude that male–female correlations in body size evolution are high, although these correlations differ among chelonian families. Overall, SSD scales isometrically with body size; Rensch's rule is valid for only one family, Testudinidae (tortoises). Because macroevolutionary patterns of SSD can vary markedly among clades, even in a taxon as morphologically conservative as Testudines, one must guard against inappropriately pooling clades in comparative studies of SSD. The results of the present study also indicate that regression models that assume the x‐variable (e.g. male body size) is measured without statistical error, although frequently reported, will result in erroneous conclusions about phylogenetic trends in sexual size dimorphism. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 108 , 396–413.     

Repeat proliferation and partial endoreplication jointly shape the patterns of genome size evolution in orchids

Although the evolutionary drivers of genome size change are known, the general patterns and mechanisms of plant genome size evolution are yet to be established. Here we aim to assess the relative importance of proliferation of repetitive DNA, chromosomal variation (including polyploidy), and the type of endoreplication for genome size evolution of the Pleurothallidinae, the most species-rich orchid lineage. Phylogenetic relationships between 341 Pleurothallidinae representatives were refined using a target enrichment hybrid capture combined with high-throughput sequencing approach. Genome size and the type of endoreplication were assessed using flow cytometry supplemented with karyological analysis and low-coverage Illumina sequencing for repeatome analysis on a subset of samples. Data were analyzed using phylogeny-based models. Genome size diversity (0.2–5.1 Gbp) was mostly independent of profound chromosome count variation (2n = 12–90) but tightly linked with the overall content of repetitive DNA elements. Species with partial endoreplication (PE) had significantly greater genome sizes, and genomic repeat content was tightly correlated with the size of the non-endoreplicated part of the genome. In PE species, repetitive DNA is preferentially accumulated in the non-endoreplicated parts of their genomes. Our results demonstrate that proliferation of repetitive DNA elements and PE together shape the patterns of genome size diversity in orchids.     

Sexual size dimorphism and sex ratios in dragonflies (Odonata)

Sexual size dimorphism and biased sex ratios are common in animals. Rensch's rule states that sexual size dimorphism (SSD) would increase with body size in taxa where males are larger than females and decrease with body size in taxa where females are larger. We tested this trend in dragonflies (Odonata) by analysing body size of 21 species and found support for Rensch's rule. The increase in SSD with increasing size among species can be explained by sexual selection favouring large males. We also estimated the slope of the relationship between sex ratio and size ratio in populations of the 21 species. A negative slope would suggest that the larger sex suffers from high mortality in the larval stage, consistent with riskier foraging. The slope of this relationship was negative, but after correcting for phylogentic non-independence with independent contrasts the relationship was no longer statistically significant, perhaps because of phylogenic inertia or low sample size.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 86 , 507–513.     

Factors shaping the evolution of colour patterns in Australian agamid lizards (Agamidae): a comparative study

Identifying general patterns of adaptive coloration in animals can help to elucidate the evolutionary processes that generate them. We examined the evolution of colour patterns in Australian agamid lizards, a morphologically and ecologically diverse group that relies primarily on visual communication. We tested whether certain types of colour (yellow–reds and black) were likely to be used as sexual signals, as indicated by their association with indices of sexual selection, namely, sexual dichromatism and sexual dimorphism in body size and head shape. We then tested whether sexually dichromatic colours are associated with specific patterns (uniform, mottled, striped, blotched, reticulated) or ecological variables such as habitat openness, arboreality, and substrate type. The presence of yellow–red on lateral and ventral body regions and black on ventral body regions was significantly more common in males than females. Lateral yellow–red in males was associated with the total extent of sexual dichromatism and size dimorphism, whereas ventral yellow–red was associated with sexual dichromatism. Both lateral and ventral yellow–red were associated with uniform patterning, suggesting that sexual signals in male agamid lizards may often comprise uniform patches or flushes of yellow–red. Although ventral black coloration was more prevalent on males (i.e. strongly sexually dichromatic), it was not associated with indices of sexual selection, suggesting that, in agamid lizards, yellow–red coloration is more likely to be sexually selected than black. Sexually dichromatic coloration was not strongly associated with any of the ecological variables measured. We found some associations, however, between female dorsal patterns and ecological variables, suggesting that female patterns are influenced by natural selection. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 101–112.     

Evaluating evolutionary pressures and phylogenetic signal in earthworms: a case study – the number of typhlosole lamellae in Hormogastridae (Annelida,Oligochaeta)

Rarely have phylogenetic comparative methods been used to study the correlation between phenotypic traits and environmental variables in invertebrates. With the widespread convergence and conservativeness of the morphological characters used in earthworms, these comparative methods could be useful to improve our understanding of their evolution and systematics. One of the most prominent morphological characters in the family Hormogastridae, endemic to Mediterranean areas, is their multilamellar typhlosole, traditionally thought to be an adaptation to soils poor in nutrients. We tested the correlation of body size and soil characteristics with the number of typhlosole lamellae through a phylogenetic generalized least squares (PGLS) analysis. An ultrametric phylogenetic hypothesis was built with a 2580‐bp DNA sequence from 90 populations, used in combination with three morphological and 11 soil variables. The best‐supported model, based on the Akaike information criterion, was obtained by optimizing the parameters lambda (λ), kappa (κ), and delta (δ). The phylogenetic signal was strong for the number of typhlosole lamellae and average body weight, and was lower for soil variables. Increasing body weight appeared to be the main evolutionary pressure behind the increase in the number of typhlosole lamellae, with soil texture and soil richness having a weaker but significant effect. Information on the evolutionary rate of the number of typhlosole lamellae suggested that the early evolution of this character could have strongly shaped its variability, as is found in an adaptive radiation. This work highlights the importance of implementing the phylogenetic comparative method to test evolutionary hypotheses in invertebrate taxa.