Incorporating an ontogenetic perspective into evolutionary theory of sexual size dimorphism

Sexual size dimorphism (SSD) describes divergent body sizes of adult males and females. While SSD has traditionally been explained by sexual and fecundity selection, recent advances in physiology and developmental biology emphasize that SSD would occur proximately because of sexual differences in ontogenetic growth trajectories (i.e., growth rate and duration). Notably, these ontogenetic traits are subject to energetic or time constraints and thus traded off with fitness components (e.g., survival and reproduction). To elucidate the importance of such ontogenetic trade‐offs in the evolution of SSD, we developed a new theoretical framework by extending quantitative genetic models for the evolution of sexual dimorphism in which we reinterpret the trait as body size and reformulate sex‐specific fitness in size‐dependent manners. More specifically, we assume that higher growth rate or longer growth duration leads to larger body size and higher reproductive success but incurs the cost of lower survivorship or shorter reproduction period. We illustrate how two sexes would optimize ontogenetic growth trajectories in sex‐specific ways and exhibit divergent body sizes. The present framework provides new insights into the evolutionary theory of SSD and predictions for empirical testing.     

Bone surface texture as an ontogenetic indicator in long bones of the Canada goose Branta canadensis (Anseriformes: Anatidae)

Growth series of femora, tibiotarsi, and humeri of the Canada goose Branta canadensis were examined to evaluate whether bone surface textures are reliable indicators of relative age and skeletal maturity in this taxon. The relationship between surface texture and skeletal maturity was analysed by comparing element texture types with both size-based and size-independent maturity estimates. A subsample of hindlimb elements was thin sectioned to observe histological structures underlying various surface textures. Three relative age classes of elements are identifiable based on surface texture. Juvenile and subadult bone textures have fibrous and/or porous areas on the bone shaft and are distinguished by the presence (in juveniles) or absence (in subadults) of coarse longitudinal striations in proximal and/or distal regions. Adult bone texture lacks surface porosity. Immature textures are caused by channels in fibrolamellar bone intersecting the bone surface; the presence or absence of striations is determined by channel orientation. Mature textures may be underlain by fibrolamellar bone with little to no surface exposure of channels, or by lamellar bone deposited after rapid growth ceases. The utility of the textural ageing method appears intimately related to the uninterrupted determinate growth regime of Branta . This suggests that bone surface textures may prove useful as skeletal maturity indicators in both modern and fossil taxa with similar growth regimes, but may not necessarily be reliable for taxa with interrupted and/or indeterminate growth.  © 2006 The Linnean Society of London, Zoological Journal of the Linnean Society , 2006, 148 , 133–168.     

Growth and textural ageing in long bones of the American alligator Alligator mississippiensis (Crocodylia: Alligatoridae)

Growth series of femora, tibiae, and humeri of the American alligator Alligator mississippiensis were examined to assess the relationship between bone surface textures and relative skeletal maturity. Element texture types were compared with both size-based and size-independent maturity estimates. Selected elements were thin sectioned to observe the histological structures underlying various surface textures. Results suggest little to no relationship between bone textures and skeletal maturity in Alligator . Controlling for additional factors suspected to affect textural variation – sexual dimorphism, seasonally interrupted growth, wild vs. captive habitat, and geographical range – provides little resolution. Indeterminate growth is almost certainly a factor; however, this alone cannot explain all observed variability. Histological analyses reveal that highly porous surface textures are often associated with zones composed of fibrolamellar bone; smoother textures are generally underlain by lamellar zones or annuli. Textures of intermediate porosity may be associated with more than one histological pattern. Until the factors affecting bone texture changes in modern crocodylians are better understood, it is recommended that the textural ageing method be applied with caution to studies of fossil archosaurs with crocodylian-like or unknown growth regimes.  © 2007 The Linnean Society of London, Zoological Journal of the Linnean Society , 2007, 150 , 1–39.     

Age,growth and maturity for two highly targeted jack species: Caranx ignobilis and Caranx melampygus

This study provides growth rate, longevity and maturity estimates for the two important species of jack in Hawaiʻi: ulua aukea/giant trevally Caranx ignobilis and omilu/bluefin trevally Caranx melampygus. Maximum observed ages for C. ignobilis and C. melampygus were 31 years and 24 years, respectively. Combined sex von Bertalanffy growth parameter values for C. ignobilis and C. melampygus were as follows: L_∞ = 1064 mm and K = 0.18 year⁻¹; and L_∞ = 718 mm and K = 0.20 year⁻¹, respectively. Female size at maturity was significantly greater than males for both C. ignobilis and C. melampygus. Size and age at maturity for C. ignobilis was 594 mm and 4.4 years for females and 465 mm and 2.8 years for males. Size and age at maturity for C. melampygus was 372 mm and 4.1 years for females and 329 mm and 2.9 years for males. This study provides the first robust demographic data for both of these highly prized and ecologically important predatory species in Hawaiʻi, which can be used for future assessments or management.     

Ecological consequences of ontogenetic changes in head shape and bite performance in the Jamaican lizard Anolis lineatopus

It has been documented extensively that body size affects the physiology and musculoskeletal function of organisms. However, less well understood is how body size affects the ecology of organisms through its effects on physiology and performance. We explored the effects of body size on morphology and performance in different ontogenetic classes and sexes of a common Anolis lizard ( A. lineatopus ). Next, we tested whether these morphological and performance differences may affect functional aspects of the diet such as prey size and prey hardness. Our data showed that males, females and juveniles differ significantly in head size, head shape and bite force. Multiple regression models indicated that head shape and bite force are significantly correlated to prey size and hardness. Yet juveniles had relatively large heads and bit disproportionately hard for their size, allowing them to eat prey as large as those of females. However, for a given prey size, males and females ate more robust prey than did juveniles. Additionally, males ate relatively harder prey than did juveniles. These data suggest that: (1) body size affects the dietary ecology of animals through its effect on head size and bite force; (2) changes in head morphology independent of changes in overall size also have important effects on performance and diet.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 443–454.     

The ontogenetic development of egg-spots in the haplochromine cichlid fish Astatotilapia burtoni

A series of Astatotilapia burtoni photographs were used to investigate the ontogenetic development of male egg-spots, a putative evolutionary key innovation of haplochromine cichlids. Four stages of egg-spot development were defined and all males had developed true egg-spots (stage 4) before reaching a standard length of 25 mm. Raising condition only slightly influenced the timing of the first appearance of true egg-spots.     

Embryogenesis and early larval development in wild-caught Levantine scraper,Capoeta damascina (Valenciennes, 1842)

Levantine scraper, Capoeta damascina is a candidate species for future stock assessments, conservation studies, and hatchery efforts. Herein, we documented embryonic and early larval development, from egg activation to the exogenous feeding period, using morphological and histological landmarks. Embryos were obtained by in vitro fertilization from hormonally induced wild-caught broodstock, and subsequent development was monitored at temperatures coinciding with native conditions. Embryonic development from fertilization to hatch lasted ~105–110 hr. Larvae emerged with unpigmented eyes and body morphology, as well as an undifferentiated digestive tract. The mouth was closed at hatch by the oropharyngeal membrane and opened by the early endogenous feeding period. Trabeculae cartilage, quadrate bone, and Meckel's cartilage of the endoskeleton were present during the endogenous feeding period. During this period, the larvae underwent considerable changes in craniofacial morphology, locomotion, and organogenesis of the digestive tract. The cartilaginous floor of the neurocranium developed and the first four ceratobranchials appeared simultaneously at the end of endogenous feeding period. The digestive tract was differentiated into buccopharynx, esophagus, and small intestine during the endogenous feeding period. The intestinal valve and numerous longitudinal folds at the posterior region of the intestine formed together by the endo–exogenous feeding period. Major developmental events in retinogenesis occurred during the endogenous feeding period. When larvae entered exogenous feeding the mouth was fully-functional. Additionally, liver size and eye diameter increased. Our analysis of embryonic and early larval development in Levantine scraper aligned with other freshwater fishes.     

The evolution of ontogenetic allometric trajectories in mammalian domestication

Morphological divergence of domesticated as compared to wild forms must result from changes in the ontogenetic process. Species‐specific tests for heterochrony have rejected a single explanation of domestic forms representing juveniles of their wild relatives. Ontogenetic allometric trajectories for 12 pairs of wild and domestic mammals were examined using skull growth data for 1070 specimens, including representatives from all lineages in which domestication has occurred. A suite of tests were performed to quantify allometric disparity in wild and domestic forms and assess the extent and patterning of modification to allometric trajectories. Domestication has modified postnatal ontogenetic allometric trajectories in mammals, and has generated disparity, achieved through lengthening of trajectory slopes and alteration to slope angles. Allometric disparity was similar for domestic forms compared to their wild relatives, whereas the magnitude of dispersion along allometric vectors differed between precocial mammals and altricial mammals, underscoring the importance of life history and shared evolutionary history in patterns of ontogenetic variation. The results verify the importance of scaling in the morphological changes associated with domestication. The response to domestication for all measured trajectory parameters was variable across species, suggesting multiple pathways of change.     

Allometry of egg and hatchling mass in birds and reptiles: roles of developmental maturity, eggshell structure and phylogeny

The factors determining hatchling mass (HM) are investigated in a wide range of birds and reptiles using regression analysis, analysis of covariance and comparative analysis by independent contrasts. In birds, initial egg mass (IEM) at laying is the most important factor affecting HM and phylogenetic relatedness has no significant effects on HM. Developmental maturity of the avian neonates did not affect the proportion of IEM converted into HM. For all reptile species, IEM also significantly affected HM but phylogenetic relatedness did not. By contrast, allometric relationships between IEM and HM in the different orders of reptiles were affected by shell type. The robustness of allometric relationships across taxa in birds and reptiles suggests that there is a physiological link between IEM and HM, which contrasts with that observed for the relationship between egg mass and incubation period. This result has significant implications for the inter-relationships between IEM and embryonic growth, which are discussed for birds and reptiles.     

Sexual maturity in young Dreissena polymorpha from Lake Como (N. Italy)

Summary

The reproductive biology of the zebra mussel Dreissena polymorpha was studied during 1999 in a natural population living in Lake Como (N. Italy), with particular reference to the differences in behavior between young and adult mussels. Histological analysis of gonads was used to study the gametogenic cycles and to evaluate when the young reached sexual maturity. Signs of active gametogenesis were detected in ≥4 mm shell length mussels. Mature gametes and the first spawning events were observed in ≥5 mm males and in ≥6 mm females. The gonad feature of ≥7 mm mussels was similar to that of the adults. Size frequency distributions revealed that the new generation (0⁺) first spawned in the year following birth, but only after winter. The length of larval time seemed to vary greatly depending on the spawning period, in addition to the environmental conditions. The first settled mussels ≥500 μm in shell length were observed 3–4 months after the first depositions. Water temperature seemed to be the most important factor which regulated sexual phenomena of both young and adult mussels. Its role in the onset of the spawning events was confirmed, but it is important to point out that temperature is not enough to trigger reproduction since gamete release is impossible without sufficient energy, especially for young mussels.     

Skeletal maturity and bone growth in twins

Heritability of skeletal maturity and bone growth is discussed on the basis of intrapair resemblances (correlation coefficients) and differences (revised percent deviations) in mono- and dizygotic twins and random pairs of unrelated children. A series of 1072 radiographs of the right hand and wrist in 63 male and 70 female pairs of monozygotic twins, and 25 male and 21 female pairs of dizygotic twins aged 12 to 18 years studied longitudinally in Tokyo were used. Skeletal maturity based on the TW2 age suggests higher heritability than bone growth based on the second metacarpal dimensions. In the latter, length has higher heritability than width and cortical thickness. A dosage effect seems to be suggested in width and some indices in the second metacarpal, but is not confirmed in skeletal maturation.     

Topographical and ontogenetic study of the neurons producing growth hormone-releasing factor in human hypothalamus

Neurons producing growth hormone-releasing factor have been characterized and analyzed by immunohistochemistry in the hypothalami of human fetuses, neonates, infants and adults, using two antibodies against human pancreatic GRF (hpGRF). One of the antibodies recognized both the hpGRF(1-40)OH and hpGRF(1-44)NH2 in the mid portion (between the 28th and 39th amino acid), the other one specifically recognized the C-terminal end of hpGRF(1-44)NH2. These two antibodies stain a single neuronal system with cell bodies mainly located in the infundibular (arcuate) nucleus, and in the ventromedial and lateralis tuber nuclei. These neurons project to the median eminence where they give numerous endings in contact with portal vessels. These neurons are distinct from those containing LH-RH, somatostatin, CRF or pro-opiocortin. In fetuses, neurons immunoreactive with hpGRF antibodies are first detected at the 29th week. They display a neuroblastic aspect which persists after birth. Immunoreactive fibers are detectable in the median eminence after the 31st week. These results demonstrate that the infundibular nucleus plays a major role in control of GH secretion in man and that secretion of GRF appears late during fetal life; this suggests that the first stages of differentiation and development of GH producing cells in the human fetus do not depend on hypothalamic GRF secretion.     

Anal‐fin ray morphology indicates sexual maturity in Brevimyrus niger (Teleostei,Mormyridae)

This osteological survey of 249 specimens of Brevimyrus niger ranging in size from 44 to 137 mm standard length (L_S) demonstrated that developmental changes in anal‐fin morphology can serve as a predictor of sexual maturity in this species. Anal‐fin ray bases begin to expand when fish reach c. 90 mm L_S at which size and above there were roughly equal numbers of individuals observed with expanded and unmodified anal‐fin bases, reflecting a 1:1 sex ratio.     

Long bone diaphyseal shape follows different ontogenetic trajectories in captive and wild gorillas

Objectives

A number of studies have demonstrated the ontogenetic plasticity of long bone diaphyseal structure in response to mechanical loading. Captivity should affect mechanical loading of the limbs, but whether captive apes grow differently than wild apes has been debated. Here, we compare captive and wild juvenile and adult Gorilla to ascertain whether growth trajectories in cross‐sectional diaphyseal shape are similar in the two environments.

Materials and methods

A sample of young juvenile (n = 4) and adult (n = 10) captive Gorilla gorilla gorilla specimens, with known life histories, were compared with age‐matched wild G.g. gorilla (n = 62) and G. beringei beringei (n = 75) in relative anteroposterior to mediolateral bending strength of the femur, tibia, and humerus. Cross sections were obtained using peripheral quantitative CT.

Results

Captive and wild adult G.g. gorilla differed in bending strength ratios for all three bones, but these differences were not present in young juvenile G.g. gorilla. In comparisons across taxa, captive juvenile G.g. gorilla were more similar to wild G.g. gorilla than to G.b. beringei, while captive adult G.g. gorilla were more similar in shape to G.b. beringei in the hind limb.

Discussion

Captive and wild G. gorilla follow different ontogenetic trajectories in long bone diaphyseal shape, corresponding to environmental differences and subsequent modified locomotor behaviors. Differences related to phylogeny are most evident early in development.

     

Body shape, diet and ontogenetic diet shifts in young fish of the Sinnamary River, French Guiana, South America

A total of 1468 young fish representing 66 taxa from the Sinnamary River, French Guiana was classified by complete cluster analysis of mean relative body width and mean relative body height into four groups. These had anguilliform, disciform, flat or intermediate body shapes and belonged chiefly to Gymnotiformes, Perciformes, Siluriformes and Characiformes, respectively. Several of the taxa shifted from one to another body shape during ontogenesis. Seven diet groups were defined by complete cluster analysis. Among these, six groups were represented by carnivorous fish. The three most frequent groups had diets of (1) mainly insect larvae and small crustaceans, (2) insect larvae, and (3) predominantly terrestrial insects. The majority of the fish taxa showed ontogenetic diet shifts. Carnivorous fish usually switched from small-size prey, such as small crustaceans, to intermediate-size prey, such as insect larvae and/or to large-size prey, such as insects and/or fish. However, taxa differed in their capacities to switch from small prey to intermediate and/or to large prey. Taxa of different body shapes had significantly different diets. Disciform fish fed mainly on aquatic insect larvae and terrestrial insects but also, in small amounts, on small curstaceans. Most anguilliform taxa ate insect larvae. Individuals belonging to the depressiform or intermediate morphotype had varied diets ranging from plant debris and substratum to fish.     

Fossil evidence of evolutionary convergence in juvenile dental morphology and upper canine replacement in sabertooth carnivores

The convergent suite of morphological traits characterizing the mammalian sabertooth ecomorphology is well documented, including modifications of the dental and osteological portions of the masticatory apparatus from a less‐specialized carnivore condition. Equally important is how those specialized adult morphologies developed through ontogeny because previous studies have shown that growing such specialized craniodental traits may require evolutionary modification of growth patterns and tooth replacement mechanisms. Despite the understanding of convergent morphological specialization in adult sabertooth carnivores, the possibility of a convergent ontogenetic trajectory toward those adult morphologies has not been rigorously examined. The present study examines numerous previously undescribed juvenile nimravid specimens. The results provide insights about nimravid ontogeny and show, for the first time, that the nimravid sabertooth lineage included species in which the permanent upper canine erupted within a lingual concavity of the deciduous upper canine until it reached comparable crown height beyond the alveolar border. Furthermore, this investigation assesses the juvenile morphology and upper canine replacement of felid and barbourofelid sabertooth taxa. The results provide evidence of convergence in deciduous upper canine morphology of three sabertooth carnivore lineages (i.e., nimravid, felid, and barbourofelid), as well as preliminary evidence of convergence in the upper canine replacement process. It might be beneficial for studies of extreme morphological specialization to simultaneously consider convergence in adult morphologies and how morphologies change through ontogeny.     

Support from early juvenile Jurassic,Cretaceous and Holocene thecideoid species for a postulated common early ontogenetic development pattern in thecideoid brachiopods

Abstract: The analysis of morphological characters exhibited by the earliest ontogenetic stages of Middle Jurassic, Cretaceous and Holocene thecideoid species, together with the application of techniques that reveal the presence of early juvenile morphological characters buried in the shell fabric of adult representatives of the species concerned, reinforce the idea of a development pattern common to thecideoids from the early Middle Jurassic to the present day. Basic and long‐standing differences in the architecture of the brachidial skeleton of thecidellinids and lacazellins may be correlated with the morphology of thecospiroids and indicate that the Thecidellinidae and Thecideidae may have emerged as sister groups as early as the Triassic.     

Studies on skeleton formation in reptiles, v. Patterns of ossification in the skeleton of Alligator mississippiensis DAUDIN (Reptilia, Grocodylia)

Patterns of ossification are described in the endo-and exoskeleton of Alligator mississippiensis. The occurrence of a dermo-supraoccipital is discussed in light of the independence of dermal and endochondral bone. The development of the bony secondary palate is discussed in light of Haeckelian recapitulation. The sequence of ossification in the limb skeleton is shown to differ from the sequence of chondrification of the cartilaginous precursors. Patterns of ossification in Alligator are compared to lepidosaurs in terms of sequence and timing. Important differences relate to ossification patterns in the limb skeleton: lepidosaurs show a dominance of digit III > IV > II > I > V, whereas Alligator shows a dominance of digits III > II> IV > I > V in the ossification process. Ontogenetic repatterning in the ossification of the axial skeleton is discussed as it bears on the serial homology of dorsal ribs, sacral ribs and caudal ribs (transverse processes).     

Size at the onset of sexual maturity in the anomuran crab, Aegla uruguayana (Aeglidae)

The size at maturity was studied in the crab Aegla uruguayana from the Areco River (31°14′ S, 59°28′ W), Argentina. Size at sexual maturity was determined according to three criteria: morphometric (change in the relative growth of reproductive characters), histological (first maturation of gonads) and functional (capability to mate and carry eggs). Regarding females, morphometric maturity occurred at a carapace length (CL) of 11.50 mm, considering abdomen width as a reproductive character. Gonad maturity of females could be observed at a minimum size ranging from 15 to 17 mm CL. The smallest ovigerous female observed in the field was 15.60 mm CL, although a relevant population incidence of ovigerous females (86.6%) has just been observed at values higher than 17 mm CL. As for males, the relative growth of the left chela length changed at a value of 15.40 mm CL, while morphological changes in sexual tube occurred between CL of 14 and 16 mm. Testicular maturation occurred at a CL ranging from 17 to 19 mm. The smallest size of males having spermatozoids in their vasa deferentia was 18.70 mm CL. The results obtained indicated that, in both sexes, functional maturity occurred after morphometric maturity and at a size similar to that of gonad maturity. Comparing sexes, females acquired sexual maturity (morphometric, gonad and functional maturity) at sizes statistically smaller than those of males.