Search

The expensive tissue hypothesis predicts a trade-off between investments in the brain and other energetically costly organs due to the costs associated with their growth and maintenance within the finite energy resources available. However, few studies address the strength of relationships between brain size and investments in precopulatory (ornaments and armaments) and postcopulatory (testes and ejaculates) sexual traits. Here, in a broad comparative study, we tested the prediction that the relationship between brain size and investment in sexual traits differs among taxa relative to the importance of sperm competition within them. We found that brain size was negatively correlated with sexual size dimorphism (SSD) in anurans and primates, and it tended to decrease with SSD in ungulates and cetaceans. However, brain size did not covary significantly with armaments (e.g., canine length, horn, antler, and muscle mass). Brain size was not correlated with postcopulatory sexual traits (testes and ejaculates). The intensity of covariance between brain size and precopulatory sexual traits decreased with increasing relative testis size.

Variation in organ structure likely provides important clues on local adaptation and reflects the pressure target of natural selection. As one of the important organs, the skin plays a key role in adapting to complex environments by reducing water loss or increasing water absorption. Nevertheless, variation in the skin structure across different populations in a single species of anurans remains enigmatic. Here, we studied geographical variation in the skin structure of male Andrew’s toads (Bufo andrewsi) across ten populations using histological methods. We quantified thickness of the skin, the epidermis, the loose layer, the compact layer, and of the epidermis, area of granular glands (GGs) and of ordinary mucous glands (OMGs), width of the calcified layer, and number of capillary vessels. We found that the thickness of the skin, dermis and loose layer in dorsal skin increased with latitude whereas the area of granular glands decreased with altitude. Moreover, the width of the calcified layer in ventral skin decreased with latitude among populations. Our findings suggest that geographical variation in skin structure in male B. andrewsi is likely to reduce water loss or make water absorption occur faster in complex high-latitude environments, improving local adaptation.

Selection pressure is an important force in shaping the evolution of vertebrate brain size among populations within species as well as between species. The evolution of brain size is tightly linked to natural and sexual selection, and life-history traits. In particular, increased environmental stress, intensity of sexual selection, and slower life history usually result in enlarged brains. However, although previous studies have addressed the causes of brain size evolution, no systematic reviews have been conducted to explain brain size in anurans. Here, we review whether brain size evolution supports the cognitive buffer hypothesis (CBH), the expensive tissue hypothesis (ETH), or the developmental cost hypothesis (DCH) by analyzing the intraspecific and/or interspecific patterns in brain size and brain regions (i.e., olfactory nerves, olfactory bulbs, telencephalon, optic tectum, and cerebellum) associated with ecological factors (habitat, diet and predator risk), sexual selection intensity, life-history traits (age at sexual maturity, mean age, longevity, clutch size and egg size, testis size and sperm length), and other energetic organs. Our findings suggest that brain size evolution in anurans supports the CBH, ETH or DCH. We also suggest future directions for studying the relationships between brain size evolution and crypsis (i.e., ordinary mucous glands in the skin), and food alteration in different developmental stages.

Sexual selection theory states that the premating (ornaments and armaments) sexual traits should trade off with the postmating (testes and ejaculates) sexual traits, assuming that growing and maintaining these traits is expensive and that total reproductive investments are limited. Male-male competition and sperm competition are predicted to affect how males allocate their finite resources to these traits. Here, we studied relative expenditure on pre- and postmating sexual traits among 82 species for three mammalian orders with varying population density using comparative phylogenetic analysis. The results showed that population density affected sexual size dimorphism (SSD) in both Artiodactyla and Carnivora, but not in Primates. However, relative testis mass and sperm size were not affected by population density. Moreover, we did not find associations between the SSD and testis mass or sperm size in three taxonomic groups. The interspecific relationships between pre- and postcopulatory sexual traits did not change with increased population density. Our findings suggest that population density did not affect variation in the relationship between pre- and postcopulatory sexual traits for these three mammalian orders.

Phenotypic flexibility of morphological and physiological traits within species is a common phenomenon across animal taxa. Hesse’s rule predicts that the size of an organ should exhibit an increase with increasing altitude along environmental gradients due to changes in oxygen supply and energy demands. Here, we test the prediction of Hesse’s rule by investigating geographical variation in the relative size of organs (i.e., heart, lungs, liver, and kidneys) across ten populations of Bufo andrewsi along an environmental gradient. We found that the relative size of these four specific organs did not increase with altitude or latitude across all populations. We also did not find that the relative size of the organs increased with increasing altitude among six populations located at a similar latitude and longitude, which is inconsistent with Hesse’s rule. Our findings suggest that oxygen supply and energy demands do not necessarily affect variation in organ size among populations.

The competition for fertilization among sperm from different males can drive variation in male reproductive investments. However, the mechanisms shaping reproductive allocation and the resulting variations in reproductive investment relative to environmental variables such as resource availability and male-male competition remain poorly known in frogs. Here, we investigated inter-population variation in male somatic condition and testis mass across four populations of the swelled vent frog Feirana quadranus along an altitudinal gradient. We found that relative testis mass did not increase with altitude, which was inconsistent with previous predictions that an increase in latitude and/or altitude should result in decreased sperm production in anurans due to shortened breeding seasons and the decline in resource availability. We also found no increase in somatic condition and male/female operational sex ratio with altitude. However, the somatic condition exhibited a positive correlation with testis mass, which indicated the condition-dependent testis size in F. quadranus. Moreover, an increase of testis mass with increasing male/female operational sex ratio suggest that male-male competition can result in an increased intensity of sperm competition, thereby increasing testis mass.

Because the brain is one of the energetically most expensive organs of animals, trade-offs have been hypothesized to exert constraints on brain size evolution. The expensive-tissue hypothesis predicts that the cost of a large brain should be compensated by decreasing size of other metabolically costly tissues, such as the gut. Here, we analyzed the relationships between relative brain size and the size of other metabolically costly tissues (i.e., gut, heart, lung, kidney, liver, spleen or limb muscles) among four Fejervarya limnocharis populations to test the predictions of the expensive-tissue hypothesis. We did not find that relative brain size was negatively correlated with relative gut length after controlling for body size, which was inconsistent with the prediction of the expensive-tissue hypothesis. We also did not find negative correlations between relative brain mass and relative size of the other energetically expensive organs. Our findings suggest that the cost of large brains in F. limnocharis cannot be compensated by decreasing size in other metabolically costly tissues.

Bergmann’s rule states that within a species of endotherms smaller individuals are found in warmer conditions, which is consistent for nearly all endotherms, while in ectotherms body size patterns are less consistent. As ectothermic vertebrates, the morphology of amphibians is likely impacted by climatic conditions. Here, we examined latitudinal variation in body size in the ranid frog, Fejervarya limnocharis, based on literature and our own data on mean body size of 3637 individuals from 50 populations and average age of 2873 individuals from 40 populations in China. The results showed that body size was positively correlated with environmental temperature, but not with precipitation. Body size was negatively correlated with latitude among populations in this species, which supported the inverse of Bergmann’s rule. Our findings suggest that a larger body size in low-latitude populations is associated with a longer growing season related to the higher environmental temperature.

The ‘cognitive buffer’ hypothesis predicts that the costs of relatively large brains are compensated for later in life by the increased benefits of large brains providing a higher chance of survival under changing environments through flexible behaviors in the animal kingdom. Thus, animals that live in a larger range (with a higher probability of environmental variation) are expected to have larger brains than those that live in a restricted geographic range. Here, to test the prediction of the ‘cognitive buffer’ hypothesis that larger brains should be expected to occur in species living in geographic ranges of larger size, we analyzed the relationship between the size of the geographic range and brain size and the size of various brain regions among 42 species of anurans using phylogenetic comparative methods. The results show that there is no correlation between relative brain size and size of the species’ geographic range when correcting for phylogenetic effects and body size. Our findings suggest that the effects of the cognitive buffer and the energetic constraints on brains result in non-significant variation in overall brain size. However, the geographic range is positively correlated with cerebellum size, but not with optic tecta, suggesting that species distributed in a wider geographic range do not exhibit larger optic tecta which would provide behavioral flexibility to allow for an early escape from potential predators and discovery of new food resources in unpredictable environments.

Brain size varies dramatically between vertebrate species. Two prominent adaptive hypotheses – the Cognitive Buffer Hypothesis (CBH) and the Expensive Brain Hypothesis (EBH) – have been proposed to explain brain size evolution. The CBH assumes that brain size should increase with seasonality, as the cognitive benefits of a larger brain should help overcoming periods of food scarcity via, for example, increased behavioral flexibility. Alternatively, the EBH states that brain size should decrease with seasonality because a smaller brain confers energetic benefits in periods of food scarcity. Here, to test the two adaptive hypotheses by studying the effects of variation in temperature and growth season on variations in overall brain size and the size of specific brain regions (viz. olfactory nerves, olfactory bulbs, telencephalon, optic tectum and cerebellum) among Hylarana guentheri populations. Inconsistent with the predictions of both the EBH and the CBH, variation in temperature and growth season did not exhibit correlations with overall brain size and the size of brain regions across populations. Hence, our data do not provide support for either the EBH or the CBH to explain brain size variation in H. guentheri. Furthermore, brain size variation did not differ between males and females in this species. Our findings suggest that both the variation in temperature and growth season did not shape the variation in brain size in H. guentheri.

Muscles are vital for the process of movement, mating and escape of predators in amphibians. During evolution, the morphological and genetic characteristics as well as the size of muscles in species will change to adapt different environments. Theory predicts that low male-male competition in high-altitude/latitude selects for small limb muscles. Here, we used the Andrew’s toad (Bufo andrewsi) as a model animal to test this prediction by analyzing geographical variation in the mass of limb muscles across nine populations from the Hengduan Mountains in China. Inconsistent with the prediction, we found that latitude and altitude did not affect the relative mass of total combined limb muscles and mass of combined hindlimb muscles among populations. Meanwhile, the relative mass of combined forelimb muscles, the two forelimb muscles (flexor carpi radialis and extensor carpi radialis) and the four hindlimb muscles (e.g. biceps femoris, semimebranous, semitendinosus and peroneus) was lowest in middle latitude and largest in low latitude whereas gracilis minor was largest in high latitudes. However, we did not find any correlations between the two forelimb muscles and the four hindlimb muscles and altitude. Our findings suggest that combined forelimb muscles, flexor carpi radialis, extensor carpi radialis, biceps femoris, semimebranous, semitendinosus and peroneus are largest in low latitudes due to pressures of mate competition.

The digestive tract provides a functional relationship between energy intake and allocation. An understanding of effects of environmental factors on the evolution of digestive tract morphology is especially important. To investigate this, we studied the variation in digestive tract length across 10 populations of the Andrew’s toad (Bufo andrewsi) between 2012 and 2015 in Sichuan province, western China. These populations were collected in different habitats varying in temperature and precipitation. The results reveal an increase in the length of the digestive tract and gut with increasing temperature and decreasing precipitation, when controlling for the effect of body size. Our findings suggest that individuals of populations living in high-temperature and low-precipitation environments have longer digestive tracts, possibly because they consume less animal-based foods and more high-fiber foods.

Competition for fertilization in multi-male group spawning can drive variation in male reproductive investment (i.e., testis mass and sperm size). Inter-population comparisons of variation in energetic availability and allocation along geographical gradients allow insights into the mechanisms shaping the reproductive investments of animals. Although inter-population differences in female reproductive investment (i.e., clutch size and egg size) have been studied extensively across a wide range of taxa, little information on variation in reproductive investment in males is available. Here, we studied altitudinal variation in testis mass and sperm length among three populations in the Jingdong tree frog (Hyla gongshanensis jingdongensis), a polyandrous species, in Yunnan Province in China. The results showed that individuals exhibited smaller testes at higher altitudes while testes mass was positively correlated with body size, body condition and age. Longer sperm length was observed in the middle-altitude population. Moreover, we found that sperm number was positively correlated with testes mass and sperm length. Our correlational findings suggest that environmental constraints at high altitude select for less investment in testes and offspring number.

Rensch’s rule describes that sexual size dimorphism (SSD) increases with body size (hyperallometry) when males are larger, and decreases with body size (hypoallometry) when males are smaller. In this paper, on the basis of mean adult body size resulting from 18 populations of the common frogRana temporariaand 24 populations of the Tibetan frogNanorana parkeri, we tested the consistency of allometric relationships between males and females with Rensch’s rule. Our results show that the variation in degree of female-biased SSD increased with increasing mean size at intraspecific levels in two species, which is consistent with the inverse of Rensch’s rule. Furthermore, we tested the hypothesis that the degree of SSD decreased with increasing altitudes. Inconsistent with the predications of our hypothesis, we found no relationships between the degree of SSD and altitude for the two species investigated. These findings suggest that females living in adverse climates in high altitudes cannot adjust their body size as plastically as males.

In many taxa, the left and right testes often differ in size. The compensation hypothesis states that an increase in size of one testis can compensate for a reduced function in the other testis. Moreover, the expensive-tissue hypothesis predicts that an increase in investment of a metabolically costly tissue is offset by decreasing investment in the other metabolically costly tissues. Here we tested these two hypotheses in Carassius auratus, by analysing difference between left and right testes mass, and between brain mass and both gut length and gonad mass (testes mass in males and clutch mass in females). We found no difference between left and right testis mass and no correlations between relative testis size and body measurements. These findings suggest that the left testis cannot serve a compensatory role. Nonetheless, contrary to the predictions of the expensive-tissue hypothesis, brain mass was positively correlated with both gut length and gonad mass within each sex. This positive correlation between brain mass and other organs (gut, gonad and clutch tissues) suggests that organisms may compensate for substantial variation in investment in tissues without sacrificing other expensive tissues.

Sexual differences in morphological traits are widespread among animals. Theory predicts that dimorphism in secondary sexual characters evolves as a consequence of sexual selection. We investigated the intersexual difference in mass of forelimb muscles of the Andrew's toad, Bufo andrewsi, an elongated species inhabiting montane regions in western China. Our results showed that average body size of females was significantly larger than males. However, when the influence of body size was removed, the forelimb muscle mass of males significantly exceeded that of females, and total mass of forelimb muscles of amplectant males was significantly larger than that of non-amplectant males. These results suggest that the robustness of the forelimbs can allow amplectant males to retain a firm grip on the female in amplexus, which may aid resistance to inference by conspecific males. Our findings are consistent with the prediction that sexual selection favors large forelimb muscle mass in males.

Elevation that results in changes in climate, duration of breeding season and food resource has long been considered a major influence on the evolution of life-history traits in amphibians. The present study examined differences in reproductive output (clutch size and egg size) of the Omei Treefrog (Rhacophorus omeimontis) at two elevations (1000 m and 1700 m above sea level) in Baoxing County, western China. Within each population, female attributes (size and age) were responsible for much of the reproductive output variation in that larger or older females produced larger clutches of smaller eggs. Clutch size and egg size showed a significantly negative correlation, which was indicative of a trade-off between the two parameters. The high-elevation females were significantly larger than the low-elevation counterparts. After accounting for interpopulational difference in body size, clutch size, egg size and clutch volume differed significantly between the populations. For the high-elevation population relatively smaller clutches tended to be associated with larger eggs. Our findings suggest that females produce smaller clutches relative to body size and larger eggs in the high-elevation population to ensure that each egg is adequately provisioned in the face of cold climate and short duration of development.

Abstract Comparative studies of the relative testes size in animals show that promiscuous species have relatively larger testes than monogamous species. Sperm competition favours the evolution of larger ejaculates in many animals – they give bigger testes. In the view, we presented data on relative testis mass for 17 Chinese species including 3 polyandrous species. We analyzed relative testis mass within the Chinese data set and combining those data with published data sets on Japanese and African frogs. We found that polyandrous foam nesting species have relatively large testes, suggesting that sperm competition was an important factor affecting the evolution of relative testes size. For 4 polyandrous species testes mass is positively correlated with intensity (males/mating) but not with risk (frequency of polyandrous matings) of sperm competition.

Abstract The age and body size of Amolops mantzorum between two populations distributed in western China were estimated using skeletochronology. The age at sexual mature of individuals was be estimated 2 yrs old in males for both populations while females reached sexual maturity at 2 yrs old at the low-altitude site and 3 yrs old at the high-altitude site. The oldest males and females from the high-altitude site were 7 yrs and 10 yrs old while longevity of males reached 6 yrs and 7 yrs in females at the low-altitude site. Average age between males and females differed significantly at the high-altitude site, but it did no differ significantly at the low-altitude site. For both sexes, average age did not differ significantly between the populations. On average, adult females had significantly larger body sizes than adult males for both populations. Sexual size dimorphism from the low-altitude site and the high-altitude site was 0.280 and 0.282, respectively. Body size between the populations differed significantly within each sex. Positive correlations were found between age and body size for both sexes within each site. The growth coefficient did not differ significantly within a population both sexes or in a sex between the populations. Our findings suggest that inter-population difference in body size of the frogs seems to be related to longevity of individuals, ambient temperature and construction of dams for electricity.