Life-history variation and allometry for sexual size dimorphism in Pacific salmon and trout

Allometry for sexual size dimorphism (SSD) is common in animals, but how different evolutionary processes interact to determine allometry remains unclear. Among related species SSD (male : female) typically increases with average body size, resulting in slopes of less than 1 when female size is regressed on male size: an allometric relationship formalized as 'Rensch's rule' . Empirical studies show that taxa with male-biased SSD are more likely to satisfy Rensch's rule and that a taxon's mean SSD is negatively correlated with allometric slope, implicating sexual selection on male size as an important mechanism promoting allometry for SSD. I use body length (and life-history) data from 628 (259) populations of seven species of anadromous Pacific salmon and trout (Oncorhynchus spp.) to show that in this genus life-history variation appears to regulate patterns of allometry both within and between species. Although all seven species have intraspecific allometric slopes of less than 1, contrary to expectation slope is unrelated to species' mean SSD, but is instead negatively correlated with two life-history variables: the species' mean marine age and variation in marine age. Second, because differences in marine age among species render SSD and body size uncorrelated, the interspecific slope is isometric. Together, these results provide an example of how evolutionary divergence in life history among related species can affect patterns of allometry for SSD across taxonomic scales.     

On the Scaling of Tooth Size in Mammals

We must establish the allometric regularities of functionalscalingin interspecific, "mouse-to elephant" plots in orderto provide criteria for the recognition of special adaptationsunrelated to the requirements of size. The qualitative literaturesuggests that postcanine tooth areas of herbivorous mammalsshould increase with positive allometry in such plots. Thispositive allometry might reflect the demands of metabolism orthe ecological strategies of large vs. small hervivores embodiedin Levins' concept of environmental grain. Plots of postcaninearea vs. body size display the expected postive allometry inall groups studied: hystricomorph rodents, suine artiodactyls(pigs, peccaries, and hippos), cervoid artiodactyls (deer, s.l),and four groups of primates considered separately (lemuroids,ceboids, cercopithecoids, and great apes). Sketchy data foraustralopithecines also indicate positive allometry and therelatively larger cheek teeth of robust forms may only reflecttheir larger body size and not the dietary differences so oftenadvocated. Phyletic dwarfs of large herbivores display negativeallometry (relatively larger cheek teeth in dwarfs) in oppositionto the interspecific trend.     

Bat genitalia: allometry, variation and good genes

Male genitalia are typically highly variable across species, for which sexual selection is thought to be responsible. Sexually selected traits characteristically show positive allometry and high phenotypic variation, although genitalia seem to be typified by negative allometry due to stabilizing selection. Additionally, while sexual selection appears to be the primary force responsible for genital evolution, the precise mechanism is unclear, but good-genes selection could be involved. If so, male genital variation should correlate with some male quality measure(s). We investigated the allometry of male Nyctalus noctula genitalia and investigated associations between genital size and three phenotypic measures of male quality (body size, relative body mass, and fluctuating asymmetry (FA)). We found that the penis exhibited positive allometry and high phenotypic variation, and was positively associated with male body size and relative body mass, but not with FA. This pattern is more typical of sexually selected display traits, contrasting with general patterns of genital allometry. The baculum was negatively allometric and was not associated with any quality measure. Our results suggest that the N. noctula penis is under directional sexual selection and is a reliable indicator of male phenotypic quality.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 83 , 497–507.     

Stoichiometry of benthic invertebrate nutrient recycling: interspecific variation and the role of body mass

Ecological stoichiometry (ES) and allometry offer frameworks for predicting how nutrient recycling varies within and among animal species. Despite the importance of benthic-derived nutrients in most aquatic systems, predictions based on ES and allometry have been poorly tested among benthic invertebrate consumers. Here, we show that the rates and ratios at which three freshwater benthic invertebrate species (a crustacean, an insect, and a polychaeta) recycled nitrogen (N) and phosphorus (P) can be partially predicted by ES and allometry depending on whether data are analyzed intra- or interspecifically. Mass-specific N and P excretion rates were negatively correlated with invertebrate body size both among and within taxa, supporting allometric predictions. However, mass-specific N and P excretion rates were positively and negatively correlated to invertebrate body N and P, respectively, but only when data were analyzed intraspecifically. As a corollary, the mass-specific N:P excretion ratio was positively related to body N:P ratio. Such a contrasting pattern on excretion-mediated N and P recycling suggests that stoichiometric constraints regarding consumer-resource imbalances for the three species utilized in this study may be stronger for P than for N. Our results indicate that the variation in nutrient recycling, which is mediated by taxonomic constraints on stoichiometry and allometry, may substantially help us to understand the importance of benthic detritivorous species to the functioning of aquatic ecosystems.     

Temperature-mediated transitions between isometry and allometry in a colonial, modular invertebrate

The evolutionary success of animal design is strongly affected by scaling and virtually all metazoans are constrained by allometry. One body plan that appears to relax these constraints is a colonial modular (CM) design, in which modular iteration is hypothesized to support isometry and indeterminate colony size. In this study, growth rates of juvenile scleractinians (less than 40mm diameter) with a CM design were used to test this assertion using colony diameters recorded annually for a decade and scaling exponents (b) for growth calculated from double logarithmic plots of final versus initial diameters. For all juvenile corals, b differed significantly among years, with isometry (b=1) in 4 years, but positive allometry (b>1) in 5 years. The study years were characterized by differences in seawater temperature that were associated significantly with b for growth, with isometry in warm years but positive allometry in cool years. These results illustrate variable growth scaling in a CM taxon and suggest that the switch between scaling modes is mediated by temperature. For the corals studied, growth was not constrained by size, but this outcome was achieved through both isometry and positive allometry. Under cooler conditions, positive allometry may be beneficial as it represents a growth advantage that increases with size.     

What Makes Vocalisation Frequency an Unreliable Signal of Body Size in Birds? A Study on Black Swans

In many animal species, the frequency (pitch) of vocalisations correlates negatively with body size and may thus signal competitive ability. However, this relationship is absent in other species. Understanding why this difference exists across species may help to explain some of the diversity of vocal communication systems. We assessed whether vocalisation frequency signals body size in black swans (Cygnus atratus), and how this is affected by (i) variation in frequency within individuals and (ii) size variation across individuals. Frequency was correlated with body size and mass, with slopes close to the allometry expected if the birds were maximising sound radiation, but the explained variation in frequency was low. Within‐individual variation in vocalisation frequency was greater in male than female swans, and the reliability of frequency as a signal of size in males was correspondingly lower. A review of the literature on the relationship between the frequency of avian vocalisations and body size also showed smaller effect sizes for more variable vocalisations (birdsongs), than for simpler vocalisations. Vocalisation frequency was more reliably correlated with body size when the sexes were pooled (creating a larger range of variation in size) than when the relationship was examined for either sex separately, although male and female data followed the same allometric line. These results show that variation in frequency within individuals and low variation in size across individuals reduce the reliability of vocalisation frequency as a signal of body size, which helps to understand differences among species in the signal value of vocalisation frequency.     

Temporal variation in body size and weapon allometry in the New Zealand giraffe weevil

1. Body size and exaggerated traits can show high phenotypic plasticity in response to environmental variation. Trait size can vary among generations but also fluctuate within a breeding season in response to resource availability. 2. This study documents patterns of temporal variation in body and weapon size, and in weapon allometry over 3 years for a wild population of New Zealand giraffe weevils [Lasiorhynchus barbicornis (Fabricius)], the males of which display an extremely elongated rostrum used as a weapon during contests for females. 3. It was predicted that body size and rostrum allometry would decrease during a breeding season, but in spite of significant annual and seasonal variation there was little evidence to support these predictions. Weapon allometry in males was more variable between years and over the breeding season than females, suggesting that male rostrum size may be more susceptible to environmental change than female rostrum size.     

Diversification, Sympatric Speciation, and Trophic Polymorphism of Arctic Charr, Salvelinus Alpinus Complex, in Transbaikalia

In northern Transbaikalia, independently evolving landlocked populations of Arctic charr are found in mountain lakes. To assess the diversity of charr in this region, speciation modes involved in the evolution of charr forms, and the role of trophic polymorphism in their divergence, we studied the morphology and feeding of dwarf, small, and large forms of Arctic charr from a number of Transbaikalian lakes. Meristic data on charr from five lakes support the earlier conclusion that the three forms do not represent separate lineages but have independently diverged in sympatry in each of the lakes. In 10 lakes, the dwarf form showed varying degrees of differentiation from normal (small and large) charr in meristic characters (up to morphologically distinct and presumably reproductively isolated groupings), which is viewed as various levels of sympatric divergence. Indexes of gill raker length in fish from 20 lakes vary among populations of both dwarf and normal charr, with forms having short and long rakers being sympatric in some of these lakes. However, the index can be used only for comparing charr of different forms up to about 32cm fork length (FL) because it is strongly negatively correlated with size in larger fish. The study of charr diets in 21 lakes indicates that large charr are piscivorous whereas dwarf and small charr feed on a wide range of invertebrates, partitioning these resources in different ways. Planktivores, including very specialized ones, and non-planktivores (benthic feeders, insectivores) can be identified within the small and dwarf forms. The proportion of plankton in the diets of dwarf and small charr is positively correlated with the number and length of gill rakers while the proportion of benthos is negatively correlated. Allopatric planktivorous and non-planktivorous small charr differ in body proportions; parallel emergence of such morphotypes in different parts of the range is a characteristic feature of the Salvelinus alpinus complex.     

Trophic structure in the pelagial of 25 shallow New Zealand lakes: changes along nutrient and fish gradients

To gain better insight into the importance of predator and resourcecontrol in New Zealand lakes we surveyed the late summer trophicstructure of 25 shallow South Island lakes with contrastingnutrient levels (6–603 µg TP l^–1) and fishdensities. Total catch of fish per net (CPUE) in multi-meshgillnets placed in the open water and the littoral zones waspositively related with the nutrient level. Trout CPUE was negativelycorrelated with total phosphorus (TP) and total nitrogen (TN).Zooplankton seemed largely influenced by fish, as high fishCPUE coincided with low zooplankton and Daphnia biomass, lowaverage weight of cladocerans, low contribution of Daphnia tototal cladoceran biomass, low ratio of calanoids to total copepodbiomass and low ratio of zooplankton biomass to phytoplanktonbiomass. However, chlorophyll a was only slightly negativelyrelated to Daphnia biomass and not to zooplankton biomass ina multiple regression that included TN and TP. Ciliate abundancewas positively related to chlorophyll a and negatively to Daphniabiomass, but not to total zooplankton biomass, while no relationshipswere found between heterotrophic nanoflagellates and zooplankton.The relationships between fish abundance and nutrients and fishabundance and zooplankton:phytoplankton ratio and between chlorophylla and TP largely followed the pattern obtained for 42 northtemperate Danish lakes. We conclude that fish, including trout,have a major effect on the zooplankton community structure andbiomass in the pelagial of the shallow oligotrophic to slightlyeutrophic New Zealand lakes, but that the cascading effectson phytoplankton and protist are apparently modest.     

It's all relative: allometry and variation in the baculum (os penis) of the harp seal, Pagophilus groenlandicus (Carnivora: Phocidae)

We compared allometry and variation in the baculum (os penis), mandible, and humerus of the harp seal, Pagophilus groenlandicus. This species is presumed to have a promiscuous mating system in which choice of mate by females during intromission with different males is likely. The baculum is large and grows throughout life so may be an honest indicator of males' quality (size) or viability (age). We predicted that bacular size would exhibit stronger allometry relative to body size than mandibles or humeri. The baculum is less functionally (mechanically) constrained than mandibles or humeri so we also predicted it would be more variable, though less variable than sexually selected traits which do not function as honest indicators. Our sample (N=67 seals) represented broad ranges of size and age (0–35 yr) so we compared variation using residuals from allometric regressions of skeletal measurements on body length. Bacular size was isometric to body length until ∼ 137 cm (when some seals enter puberty) in body length then was highly positively allometric; mandibular and humeral size were negatively allometric to body length throughout growth. Bacula were more variable than mandibles or humeri. Bacular size in large specimens (>137 cm in body length) was related strongly to body length and weakly to age. We interpret bacular size to be an uncheatable honest indicator of male quality and viability. High bacular variation conforms with theoretical predictions of females' asymmetrical choice of mate and choice of extremes, and may reflect corresponding anatomical variation among females. Some bacular variation may also result incidentally from positive allometry coupled with lifelong bacular growth, which can amplify early differences between reproductive and somatic growth, enabled by weak selection on bacular form in relation to function.     

Clutch size and body size at first reproduction in Daphnia pulicaria at different levels of food and predation

Field data from seven alpine lakes in Serra da Estrela. Portugal.show that reproduction in Daphnia may be as efficiently controlledby fish predation and copepod predation on eggs in brood cavitiesas it is by food limitation. Body length and clutch size estimatesin Daphnia pulicaria revealed high inter- and intra-populationvariability in maturation size (body size at first reproduction).and in number of eggs per clutch. Daphnia at first maturationin lakes stocked with rainbow trout were half the size of thosefound in fishless lakes (body length of 0.86–0.95 and1.55–1.81 mm. respectively). The mean number of eggs perclutch was reduced to a similar degree by food limitation, predationby fish and copepod predation on eggs in brood cavities, butthe underlying mechanisms of this reduction were different.Food limitation caused smaller clutch sizes in all individuals,so variation remained the same. Fish predation caused the selectiveremoval of individuals with maximum clutches, so variation decreased.Copepod predation caused removal of eggs from brood cavitiesof randomly infested females, so that variation increased, particularlyat a high food level when non-infested females carried largeclutches of eggs.     

Heritability of male mandible length in the stag beetle Cyclommatus metallifer

Numerous coleopteran species express male‐specific “weapon traits” that often show size variations among males, even within a single population. Many empirical studies have demonstrated that environmental conditions during development affect absolute weapon size. However, relatively few studies in horned beetles support the hypothesis that the relationship between weapon size and body size, also referred to as a “scaling relationship” or “static allometry”, is largely determined by genetic factors. In this study, the heritability of absolute mandible length and static allometry between mandible length and body size were estimated in the stag beetle Cyclommatus metallifer. While no significant heritable variation was observed in absolute mandible length, high heritability (h² = 0.57 ± 0.25) was detected in the static allometry between mandible length and body size. This is the first report on the genetic effect on male mandible size in Lucanidae, suggesting that absolute mandible size is largely determined by environmental conditions while the static allometry between weapon size and body size is primarily determined by genetic factors.     

A Test of Rensch’s Rule in Greater Horseshoe Bat (Rhinolophus ferrumequinum) with Female-Biased Sexual Size Dimorphism

Sexual size dimorphism (SSD) is widespread within the animal kingdom. Rensch’s rule describes a relationship between SSD and body size: SSD increases with body size when males are the larger sex, and decreases with body size when females are the larger sex. Rensch’s rule is well supported for taxa that exhibit male-biased SSD but patterns of allometry among taxa with female-biased size dimorphism are mixed, there is evidence both for and against the rule. Furthermore, most studies have investigated Rensch’s rule across a variety of taxa; but among-population studies supporting Rensch’s rule are lacking, especially in taxa that display only slight SSD. Here, we tested whether patterns of intraspecific variation in SSD in greater horseshoe bats conform to Rensch’s rule, and evaluated the contribution of latitude to Rensch’s rule. Our results showed SSD was consistently female-biased in greater horseshoe bats, although female body size was only slightly larger than male body size. The slope of major axis regression of log₁₀ (male) on log₁₀ (female) was significantly different from 1. Forearm length for both sexes of greater horseshoe bats was significantly negatively correlated with latitude, and males displayed a slightly but nonsignificant steeper latitudinal cline in body size than females. We suggest that variation in patterns of SSD among greater horseshoe bat populations is consistent with Rensch’s rule indicating that males were the more variable sex. Males did not have a steeper body size–latitude relationship than females suggesting that sex-specific latitudinal variation in body size may not be an important contributing factor to Rensch’s rule. Future research on greater horseshoe bats might best focus on more comprehensive mechanisms driving the pattern of female-biased SSD variation.     

Quantitative genetic variation in static allometry in the threespine stickleback

The common pattern of replicated evolution of a consistent shape-environment relationship might reflect selection acting in similar ways within each environment, but divergently among environments. However, phenotypic evolution depends on the availability of additive genetic variation as well as on the direction of selection, implicating a bias in the distribution of genetic variance as a potential contributor to replicated evolution. Allometry, the relationship between shape and size, is a potential source of genetic bias that is poorly understood. The threespine stickleback, Gasterosteus aculeatus, provides an ideal system for exploring the contribution of genetic variance in body shape allometry to evolutionary patterns. The stickleback system comprises marine populations that exhibit limited phenotypic variation, and young freshwater populations which, following independent colonization events, have often evolved similar phenotypes in similar environments. In particular, stickleback diversification has involved changes in both total body size and relative size of body regions (i.e., shape). In a laboratory-reared cohort derived from an oceanic Alaskan population that is phenotypically and genetically representative of the ancestor of the diverse freshwater populations in this region, we determined the phenotypic static allometry, and estimated the additive genetic variation about these population-level allometric functions. We detected significant allometry, with larger fish having relatively smaller heads, a longer base to their second dorsal fin, and longer, shallower caudal peduncles. There was additive genetic variance in body size and in size-independent body shape (i.e., allometric elevation), but typically not in allometric slopes. These results suggest that the parallel evolution of body shape in threespine stickleback is not likely to have been a correlated response to selection on body size, or vice versa. Although allometry is common in fishes, this study highlights the need for additional data on genetic variation in allometric functions to determine how allometry evolves and how it influences phenotypic evolution.     

The growth of young pike in small Finnish lakes with different acidity-related water properties and fish species composition

Pike growth was generally slower in small Finnish lakes than has been reported from large lakes or brackish coastal waters. Growth was unrelated to pH, alkalinity, COD, or conductivity of the water, but length of 1–2-year-old pike correlated positively with water colour (i.e. humic content), nitrogen content, and phosphorus content. These water properties also correlated with each other. Growth of 1–2-year-old pike was negatively correlated with lake area in lakes smaller than 20 ha.
In lakes with a strong roach population or without ruffe the 0 group pike grew faster than in lakes without roach or with ruffe. The growth of pike aged 1–4 years in two very acid and practically fishless lakes did not differ clearly from the rest of the lakes, although the pike were forced to forage for abundant acid resistant invertebrates like dragonfly nymphs (Odonata) or Asellus aquatlcus .
The results of this work support earlier studies where the growth rate above all depends on water temperature and food availability. Acidity was not shown to affect the growth rate of pike.     

Static intraspecific allometry of the dentition in Otoletnur crassicaudatus

Adult static intraspecific allometry of tooth size was evaluated in a sample of 66 Otolemur crassicaudatus (34 male, 32 female). Tooth areas were calculated from mesiodistal and buccolingual measurements of canines and postcanine teeth of both arcades and were scaled to four viscerocranial measurements: bimaxillary width; maxillo-alveolar length; mandibular length and bigonial width. Individual tooth crown areas were also scaled to total skull length, body length and body weight. From the log-transformed analyses it is concluded that postcanine tooth size was unrelated to body length or weight, and poorly correlated to skull length or jaw size. Although viscerocranial size appears to be independent of body size, these measures are well correlated to skull length. It is shown that the longer the skull, the shorter and narrower the maxilla, and the longer and broader the mandible. Canines are shown to scale negatively allometric to skull length, hence, large animals will have relatively small canines.     

The scaling of basicranial flexion and length.

Based on correlations between the cranial base angle (CBA) and the index of relative encephalization (IRE, calculated as the cubed root of brain volume divided by basicranial length), several recent studies have identified relative brain size as the factor most responsible for determining basicranial flexion in primates. IRE, however, scales with positive allometry relative to body mass, unlike the negatively allometric relationship between brain volume and body mass. This poses new questions concerning the factors underlying the correlation between IRE and CBA. Specifically, if basicranial flexion represents a spatial solution to the problem of housing a large brain within a neurocranium of limited size, then why is it that the problem is greatest in those species whose brains are smallest relative to body mass? To address this question, the scaling relationships of IRE and the measurements used to calculate it were examined in 87 primate species. It was found that the positive allometry of IRE is due to the fact that its denominator, basicranial length (BL), scales with very strong negative allometry relative to body mass. The scaling relationship of BL may reflect the fact that the noncortical components of the brain (i.e., diencephalon, mesencephalon, medulla) also scale with strong negative allometry relative to body mass, perhaps because of energetic constraints. Importantly, BL and these three brain components scale isometrically against each other. Thus, although cranial base flexion may be an adaptation to accommodate the size of the brain relative to basicranial length, the reason why that adaptation is necessary is not the evolution of a large brain, but rather the evolution of a short cranial base. In so far as basicranial length is affected by the strong negative allometry of the diencephalon, mesencephalon and medulla, the scaling relationships of these brain components are therefore indirectly responsible for the evolution of basicranial flexion.     

Evolution of group size in the dolphins and porpoises: interspecific consistency of intraspecific patterns

I investigated group size variability in dolphins and porpoisesusing intraspecific comparisons. Explanatory factors consideredin the analysis were variables of the physical environment,the diet, and the life history of the species. Open habitatand small body size were viewed as increasing predation risk.This pattern was apparent in Risso's dolphins (Grampus griseus) and weakly apparent in bottlenose dolphins (Tursiops spp.).Group size was negatively correlated with body size in pilotwhales (Globicephala spp.) and positively correlated with theopenness of habitat in killer whales (Orcinus orca), stripeddolphins (Stenella coeruleoalba), and common dolphins (Delphinus spp.). No such relationship was found for harbor and Dall'sporpoises (Phocoena phocoena, P. dalli). Group size also seemedto vary depending on other physical measures of the habitat,which may indirectly reflect diet; group size showed U-shapedpatterns if related to temperature. The predictive power ofvariables comprising detailed prey information on group sizewas variable. For example, pilot whales had smaller group sizes when they fed more on mesopelagic fish and less on mesopelagiccephalopods, and common dolphins had larger groups if theyfed on varying types of fish. In most Delphinoidea species,group size could be described by the variables considered inthis study. But each species showed its own pattern of correlationsbetween group size and a specific set of explanatory variables. Thus, no general and consistent relation between group sizeand the other variables was found. It remains unknown whetherthese species-specific patterns result from a historical processor whether they are specialized adaptations.     

Allometry of reaching and contact structures in Kukulcania hibernalis (Araneae: Filistatidae)

Large part of the morphological diversity observed across taxa is attributed to the effect of sexual selection; and the static allometry of these structures vary largely from highly positive to negative, depending on their function, and position on the animal's body. In arthropods, information of how sexually selected contact and reaching male structures use during courtship scale on body size is scarce. We tested two complementary hypotheses: the reaching structure hypothesis and the contact‐function hypothesis, in the spider Kukulcania hibernalis. We used the length of the proximal segments of the male pedipalp to test the reaching structure hypothesis, and claw features to test the contact‐function hypothesis. Our results support both hypotheses. Small males have disproportionally longer pedipalps (highly negative allometry) than large males, increasing the probability of small‐bodied males to inseminate even large females. We also found that both distal contact and noncontact homologous structures scaled shallow (slope < 1) on body size, but allometry was significantly shallower for contact than for noncontact distal structures, providing support to the contact‐function hypothesis, and allowing teasing apart the effect of sexual selection on distal contact structures with dual functions.     

Parallel divergence of sympatric genetic and body size forms of Arctic charr,Salvelinus alpinus,from two Scottish lakes

F _ST and R_ST estimates for Arctic charr from six microsatelite markers collected from two neighbouring Scottish lakes, Loch Maree and Loch Stack, confirm the presence of two distinct genetic groupings representing separate populations within each lake. In both lakes, there was also a clear body size dimorphism, with large and small body size forms that segregated according to genetic grouping. There was evidence of only subtle foraging ecology differences between morphs, with the small body size morph in both lakes being more generalist in its foraging in the summer (consuming mostly plankton but also some macrobenthos) than the large body size morph, which specialized on planktonic prey. Trophic morphology (head and mouth shape) did not differ significantly between morphs (although the small sample size for Maree makes this a preliminary finding). Cluster analysis of the microsatelite data and the presence of private alleles showed that morphologically similar forms in different lakes were not genetically similar, as would be expected under a multiple invasion hypothesis. Thus, the data do not support a hypothesis of a dual invasion of both lakes by two common ancestors but instead suggest an independent origin of the two forms in each lake. Thus parallel sympatric divergence as a result of common selection pressures in both lakes is the most parsimonious explanation of the evolutionary origin of these polymorphisms. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 748–757.