Golden Orbweavers Ignore Biological Rules: Phylogenomic and Comparative Analyses Unravel a Complex Evolution of Sexual Size Dimorphism.

Sexual size dimorphism varies substantially among populations and species but we have little understanding of the sources of selection generating this variation. We used path analysis to study how oviposition host affects selection on body size in a seed-feeding beetle (Stator limbatus) in which males contribute large ejaculates (nuptial gifts) to females. Females use nutrients in these ejaculates for egg production. Male body size, which affects ejaculate size, affects female fecundity and is thus under fecundity selection similar in magnitude to the fecundity selection on female body size. We show that when eggs are laid on a host on which larval mortality is low (seeds of Acacia greggii) fecundity predicts fitness very well and fecundity selection is the major source of selection on both male and female adult size. In contrast, when eggs are laid on a host on which larval mortality is high (seeds of Parkinsonia florida) fecundity poorly predicts fitness such that fecundity selection is relaxed on both male and female size. However, because egg size affects larval mortality on this poor host (P. florida) there is selection on female size via the female size --> egg size --> fitness path; this selection via egg size offsets the reduction in fecundity selection on female, but not male, body size. Thus, differences in host suitability (due to differences in larval mortality) affect the relative importance of two sources of selection on adult body size; fecundity selection on both male and female body size is lower on the poor quality host (P. florida) relative to the high quality host (A. greggii) whereas selection on female body size via effects of egg size on offspring survival (body size --> egg size --> fitness) is greater on the poor quality host relative to the high quality host. Because selection via the egg size path affects only females the difference in larval survival between hosts shifts the relative magnitude of selection on female vs. male size. Researchers working on other study systems should be alerted to the possible importance of subtle, but consequential, indirect selection on their study organisms.

Empirical evidence suggests that Rensch's rule of allometric scaling of male and female body size, which states that body size divergence is greater across males than across females of a clade, is not universal. In fact, quantitative genetic theory indicates that the sex under historically stronger directional selection will exhibit greater interspecific variance in size. Thus, the pattern of covariance between allometry of male and female body size and sexual size dimorphism (SSD) across related clades allows a test of this causal hypothesis for macroevolutionary trends in SSD. We compiled a data set of published body size estimates from the amphibians, a class with predominantly female-biased SSD, to examine variation in allometry and SSD among clades. Our results indicate that females become the more size-variant sex across species in a family as the magnitude of SSD in that family increases. This rejects Rensch's rule and implicates selection on females as a driver of both amphibian allometry and SSD. Further, when we combine our data into a single analysis of allometry for the class, we find a significant nonlinear allometric relationship between female body size and male body size. These data suggest that allometry changes significantly as a function of size. Our results illustrate that the relationship between female size and male size varies with both the degree of sexual dimorphism and the body size of a clade.

Females are larger than males in most invertebrate taxa, a phenomenon believed to result from the pressures exerted on female body size by size-dependent fecundity. Male-male competition, which can act on male body size, is not thought to play as important a role in the evolution of sexual size dimorphism in invertebrates as it apparently does in some vertebrate groups. Here, using a comparative approach, the relationship between sexual size dimorphism and adult sex ratio is examined across 46 natural populations (41 species) and 30 experimental populations (21 species) of parasitic nematodes. If male-male competition via physical contests is important, relative male size should increase as the sex ratio becomes less female-biased. This is exactly what was found in the analyses, where residuals of male size regressed on female size were used as measures of sexual size dimorphism. This result was independent of any phylogenetic influences, and was obtained for both natural and experimental nematode populations. In addition, there was no evidence of any Allometric relationship between male and female body size. The average ratio of male size to female size was roughly constant across all species and independent of body size. The results are consistent with a role for male-male competition in explaining specific deviations from the average ratio of male to female body size, suggesting a significant role for sexual selection in the evolution of nematode body sizes.

Covariation of sexual size dimorphism and adult sex ratio in parasitic nematodes

Map turtles and sawbacks (Emydidae: Deirochelyinae: Graptemys) are a diverse group of turtles that are of ecological interest due to their diversity in trophic morphology, particularly in females, and their extreme sexual size dimorphism (with females larger). I used comparative analyses (independent contrasts in correlation analyses and GLM analyses) to examine hypotheses regarding the evolution of body size in the genus. Evolutionary changes in body size of both males and females were positively related to inferred shifts in latitude. Trophic morphology (relative head width, expressed either as a continuous or a discrete variable) was not an additive source of variation in male body size, but was for female body size, primarily due to the large body sizes exhibited by the megacephalic southern clade (G. pulchra, G. ernsti, G. gibbonsi, and G. barbouri). Status as allopatric or sympatric to other species of Graptemys was not an additive source of variation in female body size. These results argue against the hypothesis that character displacement of body size in females was important in the radiation of map turtle and sawback species and instead suggest a functional relationship whereby degree of molluscivory in females covaries with body size. Sexual size dimorphism was found to increase with body size of females, also due primarily to the large females of the megacephalic clade; this result means Graptemys is an exception to Rensch's Rule. In a latitude-corrected analysis of body size evolution in deirochelyine turtles, the exceptional degree of sexual size dimorphism in Graptemys appears to result more from reduction in male size than increase in female size. Decreased male size may indicate relaxed selection for large body size in Graptemys males as a consequence of the fact that they rarely leave the water for terrestrial excursions, because selection for larger male body size in other deirochelyines may be mediated by (a) predation pressure imposed by terrestrial predators, (b) enhancement of overland mobility for mate searching, and (c) the need for resistance to desiccation during overland excursions. Alternatively, male body size reduction in Graptemys may be explained by energetic requirements of searching for mates in the fluvial environment or unknown differences in social structure among deirochelyine turtles.

Body size is one of the most important quantitative traits under evolutionary scrutiny. Sexual size dimorphism (SSD) in a given species is expected to result if opposing selection forces equilibrate differently in both sexes. We document variation in the intensity of sexual and fecundity selection, male and female body size, and thus SSD among 31 and 27 populations of the two dung fly species, Scathophaga stercoraria and Sepsis cynipsea, across Switzerland. Whereas in S. cynipsea females are larger, the SSD is reversed in S. stercoraria. We comprehensively evaluated Fairbairn and Preziosi's (1994) general, three-tiered scenario, hypothesizing that sexual selection for large male size is the major driving force of SSD allometry within these two species. Sexual selection intensity on male size in the yellow dung fly, S. stercoraria, was overall positive, greater, and more variable among populations than fecundity selection on females. Also, sexual selection intensity in a given population correlated positively with mean male body size of that population for both the field-caught fathers and their laboratory-reared sons, indicating a response to selection. In S. cvnipsea, sexual selection intensity on males was lower overall and significantly positive, about equal in magnitude, but more variable than fecundity selection on females. However, there was no correlation between the intensity of sexual selection and mean male body size among populations. In both species, the laboratory-reared offspring indicate genetic differentiation among populations in body size. Despite fulfillment of all key prerequisites, at least in S. stercoraria, we did not find hypoallometry for SSD (Rensch's rule, i.e., greater evolutionary divergence in male size than female size) for the field-caught parents or the laboratory-reared offspring: Female size was isometric to male size in both species. We conclude that S. cynipsea does not fit some major requirements of Fairbairn and Preziosi's (1994) scenario, whereas for S. stercoraria we found partial support for it. Failure to support Rensch's rule within the latter species may be due to phylogenetic or other constraints, power limitations, erroneous estimates of sexual selection, insufficient genetic isolation of populations, or sex differences in viability selection against large size.

Rensch's rule predicts an allometric relationship between male and female body size stating that the sexual size dimorphism (SSD) increases with body size in male-larger taxa and decreases in female-larger taxa in groups of related species. It means that the relationship between the male and female body size is hyperallometric, i.e., the allometric exponent of this relationship exceeds the unity. We explored the relationship between the male and female body size in a New World clade of lizards consisting of sister families Teiidae and Gymnophthalmidae, which exhibit a great variation in both their adult body sizes and SSD. All our estimates of the reduced major axis regression slopes ranged from 1.067 to 1.229 and clearly followed a pattern consistent with the Rensch's rule. Despite a clear general trend, giant species from the subfamily Tupinambinae show paradoxically only poor SSD. The cases of extreme male-larger SSD were found in species of moderate body size belonging to the genera Ameiva and Cnemidophorus. The abovementioned deviations from the hyperallometric relationship between the male and female body size are surprising and require further examination.

In sexually reproducing animals, the process of mate choice by females is often mixed with the process of male-male competition. Current models of female male choice focus mainly on how females identify the higher quality of males, but neglect the effect of male-male competition on the mate choice of females. Therefore, it remains controversial what is the relative importance of two processes in forming a social bond. We propose a new 'trial marriage' model for females' mate choice. The model assumes that females unconditionally accept any male they first encounter as their mating partner, and then conditionally switch mates to a new male of higher quality than their current partner when male-male competition occurs. This model was tested in the green weevil Hypomeces squamosus by exploring how females switched mates when males' mating interference was experimentally induced. The likelihood that females switched mates, as well as their conditional acceptance criteria of a new mate, was both raised with the intensity of males' mating interference that was manipulated in an enhanced encounter rate experiment, and in male introduction or stepwise removal experiments. These experimental findings confirm that a 'trial marriage' strategy occurs during females' mate choice. Compared with other strategies, it is more beneficial for females to choose a better mate without paying the costs of identifying males as suggested by the 'trial marriage' strategy. More importantly, using the current partner quality as the conditional acceptance threshold of new mates, females can choose better males in future encounters with potential mates. In the green weevils, males' preference for larger females and the higher possibility of the largest male winning an interference are mixed together when males' mating interference reaches a higher intensity. Therefore, the consequence of a male interference will determine which male could be chosen by a female. Under this condition, conditional acceptance of the winner becomes the most beneficial strategy of females in choosing their mates. We thus suggest that the 'trial marriage' strategy would be more efficient when males' mating interference becomes the determinant factor of females' mate choice.

Rensch’s rule describes a pattern of allometry in sexual size dimorphism (SSD): when males are the larger sex (male-biased SSD), SSD increases with increasing body size, and when females are the larger sex (female-biased SSD), SSD decreases with increasing body size. While this expectation generally holds for taxa with male-biased or mixed SSD, examples of allometry for SSD consistent with Rensch’s rule in groups with primarily female-biased SSD are remarkably rare. Here, I show that the majority of dwarf chameleons (Bradypodion spp.) have female-biased SSD. In accordance with Rensch’s rule, the group exhibits an allometric slope of log(female size) on log(male size) less than one, although statistical significance is dependent on the phylogenetic comparative method used. In this system, this pattern is likely due to natural selection on both male and female body size, combined with fecundity selection on female body size. In addition to quantifying SSD and testing Rensch’s rule in dwarf chameleons, I discuss reasons why Rensch’s rule may only rarely apply to taxa with female-biased SSD.

Bergmann's and Rensch's rules describe common large-scale patterns of body size variation, but their underlying causes remain elusive. Bergmann's rule states that organisms are larger at higher latitudes (or in colder climates). Rensch's rule states that male body size varies (or evolutionarily diverges) more than female body size among species, resulting in slopes greater than one when male size is regressed on female size. We use published studies of sex-specific latitudinal body size clines in vertebrates and invertebrates to investigate patterns equivalent to Rensch's rule among populations within species and to evaluate their possible relation to Bergmann's rule. Consistent with previous studies, we found a continuum of Bergmann (larger at higher latitudes: 58 species) and converse Bergmann body size clines (larger at lower latitudes: 40 species). Ignoring latitude, male size was more variable than female size in only 55 of 98 species, suggesting that intraspecific variation in sexual size dimorphism does not generally conform to Rensch's rule. In contrast, in a significant majority of species (66 of 98) male latitudinal body size clines were steeper than those of females. This pattern is consistent with a latitudinal version of Rensch's rule, and suggests that some factor that varies systematically with latitude is responsible for producing Rensch's rule among populations within species. Identifying the underlying mechanisms will require studies quantifying latitudinal variation in sex-specific natural and sexual selection on body size.

Female-biased sexual size dimorphism is uncommon among vertebrates and traditionally has been attributed to asymmetric selective pressures favoring large fecund females (the fecundity-advantage hypothesis) and/or small mobile males (the small-male advantage hypothesis). I use a phylogenetically based comparative method to address these hypotheses for the evolution and maintenance of sexual size dimorphism among populations of three closely related lizard species (Phrynosoma douglasi, P. ditmarsi, and P. hernandezi). With independent contrasts I estimate evolutionary correlations among female body size, male body size, and sexual size dimorphism (SSD) to determine whether males have become small, females have become large, or both sexes have diverged concurrently in body size during the evolutionary Xhistory of this group. Population differences in degree of SSD are inversely correlated with average male body size, but are not correlated with average female body size. Thus, variation in SSD among populations has occurred predominantly through changes in male size, suggesting that selective pressures on small males may affect degree of SSD in this group. I explore three possible evolutionary mechanisms by which the mean male body size in a population could evolve: changes in size at maturity, changes in the variance of male body sizes, and changes in skewness of male body size distributions. Comparative analyses indicate that population differentiation in male body size is achieved by changes in male size at maturity, without changes in the variance or skewness of male and female size distributions. This study demonstrates the potential of comparative methods at lower taxonomic levels (among populations and closely related species) for studying microevolutionary processes that underlie population differentiation.

Sexual size dimorphism (SSD), a difference in body size between the sexes, occurs in many animal species. Although the larger sex is often considered invariable within species, patterns of selection may result in interpopulation variation or even reversal of SSD. We evaluated correlations between latitude and female body size, male body size, and relative body size (male body size/female body size) in 22 populations (ranging from 37 degrees N to 49 degrees N) of sea-run masu salmon (Oncorhynchus masou) that spawn in rivers along the Sea of Japan coast. Male size and the relative body size increased with latitude, but female size did not correlate with latitude. In addition, increase in male size with latitude was sufficient to result in a reversal of SSD, the switch-point being around 45 degrees N. We suggest that the positive correlation between latitude and male size is due to increasing operational sex ratios or sexual selection on sea-run male body size that result from sex-biased patterns of anadromy. In conclusion, our study provides the first example of predictable geographic variation in SSD shaped by apparent patterns of sexual selection.

Sexual dimorphism is commonly used to directly infer or support reconstructions of social behavior in early hominins. This is often done by comparing the magnitude of sexual size dimorphism to that seen in extant primates and extrapolating a likely social behavior. Such comparisons are of limited value, though, allowing only the inference of strong male–male competition when dimorphism is strong. Recent studies have begun to focus on the selective factors that impact female body size, and thereby size dimorphism. Considerations of changes in male and female size in the fossil record potentially allow insight into the meaning of changes in sexual dimorphism through time. To illustrate, I compare estimates of body mass dimorphism for four hominin taxa to assess changes in male and female size. Assuming that early Homo represents a single taxon, sexual size dimorphism increased in early Homo through an increase in male size, but was subsequently reduced through an increase in female size in Homo erectus. This would imply a significant increase in sexual selection acting on males in early Homo. An increase in female size with a loss of dimorphism in Homo erectus would imply a simultaneous shift in female optimal body size through selection for increased female fecundity, and/or an increase in female resource abundance, coupled with a shift in selection acting on male size. Although none of these inferences are certain, the exercise illustrates the potential for considering how dimorphism changes through time, rather than simply focusing on the magnitude of size dimorphism in isolation.

After copulation, male grasshoppers of Sphenarium purpurascens (Orthoptera: Pyrgomorphidae) remain in a postinsemination association with their mate. A male can spend as many as 17 days mounted on a female. Guarding duration is related to both male and female body size and the female's mating history. Longest guarding durations were recorded at the middle of the reproductive season, when the probability of encounter between the sexes (sex ratio and population density) was decreasing, at the beginning of the associated dry season. These guardings were associated with large individuals of both sexes and with females that had more previous partners. Moreover, a positive association was found among guarding duration, female and male body size and age, and number of copulations performed by the males. Maybe males invest time and sperm in females as a function of the probability of sperm competition. Nevertheless, guarding may provide benefits to both sexes. Males may reduce the possibility of sperm competition, and females may obtain nutritional benefit for themselves or their offspring as a result of multiple copulations. Changes in male investment in guarding duration and number of copulations may be the result of physiological constraints related to seminal and/or sperm production. Moreover, guarding duration could be constrained by ecological factors such as a reduction of food availability associated with the beginning of the dry season.

Female body size is more sensitive to the environmental conditions during development than male body size in many insect species with female-biased sexual size dimorphism (SSD) (i.e., females are larger than males). However, the sexual difference in body size plasticity is largely unknown in species with male-biased SSD. Here, I conducted a laboratory experiment using low- and high-quality diets to examine sexual differences in body size plasticity in the male-larger rhinoceros beetle Trypoxylus dichotomus Linnaeus, 1771 (Coleoptera: Scarabaeidae). I found that male body size was much more greatly affected by nutritional status than female body size. The stronger condition dependency in male body size is likely associated with sexual selection for male body size. Furthermore, in wild-caught beetles, males showed larger body size differences between years within populations, while the body size of females was more constant. Within populations and years, male body size also showed greater variation than female body size. In addition, SSD of field-caught beetles was usually much smaller than that of lab-reared beetles of corresponding populations. Thus, the stronger condition dependency of male body size in this species probably has profound effects on the variation of observed body size and SSD among and within populations.