Heterochronic Shifts Research Articles

Heterochrony and post‐natal growth in mammals – an examination of growth plates in limbs

Mammals display a broad spectrum of limb specializations coupled with different locomotor strategies and habitat occupation. This anatomical diversity reflects different patterns of development and growth, including the timing of epiphyseal growth plate closure in the long bones of the skeleton. We investigated the sequence of union in 15 growth plates in the limbs of about 400 specimens, representing 58 mammalian species: 34 placentals, 23 marsupials and one monotreme. We found a common general pattern of growth plate closure sequence, but one that is universal neither between species nor in higher-order taxa. Locomotor habitat has no detectable correlation with the growth plate closure sequence, but observed patterns indicate that growth plate closure sequence is determined more strongly through phylogenetic factors. For example, the girdle elements (acetabulum and coracoid process) always ossify first in marsupials, whereas the distal humerus is fused before the girdle elements in some placentals. We also found that heterochronic shifts (changes in timing) in the growth plate closure sequence of marsupials occur with a higher rate than in placentals. This presents a contrast with the more limited variation in timing and morphospace occupation typical for marsupial development. Moreover, unlike placentals, marsupials maintain many epiphyses separated throughout life. However, as complete union of all epiphyseal growth plates is recorded in monotremes, the marsupial condition might represent the derived state.

Cranial Suture Closure Patterns in Sciuridae: Heterochrony and Modularity

Studies of sequence heterochrony in mammalian evolution have revealed differences in bone ossification between and within major clades. Sequences of late stage developmental events have been less well studied, and the relation of modularity to sequence heterochrony at these stages has not been explicitly tested. Here, the first data on cranial suture closure are provided for members of Sciuridae. Sequence heterochrony is quantified using the recently developed Parsimov-based genetic inference (PGi) algorithm to identify shifts in suture closure sequence, and modularity in heterochronic shifts is tested. Results indicate that suture closure pattern was quite variable among sciurids, and interspecific correspondence in closure sequence was generally lower than has been found for other rodents, and for carnivorans. A number of sequence heterochronies were detected for inclusive clades, and these were not randomly distributed but mainly concentrated among sutures that exhibited high rank variability and belonged to the orbit and cranial vault modules, suggesting that some regions of the cranium exhibited a greater capacity for variation in suture closure. Heterchronies were not detected for sutures belonging to the basicranium, or anterior orbit-nasal modules, both of which are recognized as highly integrated modules based on landmark data. Modularity of suture closure sequence was not significant for any modules following multiple-comparison correction, which contrasts with modularity that has been recovered in early stage, ossification sequence events among other mammals.

Timing of cranial suture closure in placental mammals: Phylogenetic patterns, intraspecific variation, and comparison with marsupials

Used as markers of postnatal growth closure sequences of 22 ectocranial sutures and synchondroses were recorded in a sample of 1161 skulls belonging to 38 species from all major placental clades: Afrotheria, Xenarthra, Laurasiatheria and Euarchontoglires (Boreoeutheria). The maximum closure level, which is not significantly correlated to body mass, is higher in Afrotheria and Xenarthra than in Boreoeutheria. Only the basioccipito-basisphenoid and the basioccipito-exoccipital synchondroses close in all species sampled, the supraoccipito-exoccipital and the inter-parietal sutures do in most species. Parsimov retrieved more heterochronic shifts for Afrotheria and Xenarthra than for Boreoeutheria. The amount of intraspecific variation differs among the species sampled being high among xenarthran species and low among afrotherians. Specimens (162) representing 12 marsupial genera were also analysed. Placentals exhibit a larger number of suture closures than marsupials and in both groups the sutures at the base of the skull are the first to fuse starting with the basioccipito-exoccipital.

Reproductive and morphometric traits of <i>Macrobrachium amazonicum</i> (Decapoda: Palaemonidae) from the Pantanal, Brazil, suggests initial speciation

The palaemonid shrimp Macrobrachium amazonicum shows an unusually large geographic range (ca. 4000km across) living in coastal, estuarine, and limnic inland habitats of the upper Amazon, Orinoco, and La Plata basins. This raises doubts whether allopatric, ecologically diverse populations belong to the same species. While shrimps from estuarine and Amazonian habitats have been studied in great detail, very little is known about hololimnetic inland populations. In the present study, biological traits related to growth (maximum body size, fresh weight, morphometric relationships) and reproduction (sex ratio; occurrence of male morphotypes; minimum sexable size; minimum size of ovigerous females; fecundity; egg size), were studied in M amazonicum collected from a pond culture and two natural freshwater habitats (Rio Miranda; Lagoa Baiazinha) in the Pantanal of Mato Grosso do Sul, Brazil. In total, 2270 shrimps were examined (603 males; 1667 females, 157 of these ovigerous). Sex ratio (males:females) was at all sampling sites strongly female-biased, ranging from 0.2-0.6. Maximum body size was larger in natural habitats compared to the pond culture, suggesting reduced growth or a shorter life span under artificial mass rearing conditions. Maximum fecundity observed in our material was 676 eggs, reached by the largest female (TL=65mm; Lagoa Baiazinha). A significant difference between slope parameters of linear regressions describing fecundity, either in terms of numbers of eggs laid or of larvae released, in relation to female fresh weight, indicates egg losses. This may be due in part to a 2.4-fold increase in egg volume occurring during the course of embryonic development, while the available space under the abdomen remains limited. Size-weight relationships differed significantly between males and females, indicating sexspecific morphometric differences. Males appear to have a more slender body shape than females, reaching thus lower weight at equal TL. When reproductive and morphometric traits are compared with literature data from estuarine and inland populations living in the Amazon and Orinoco plains, shrimps from the Pantanal show conspicuous peculiarities differing from other populations: (1) maximum body size is far smaller, suggesting shorter longevity; (2) females are consistently larger than males; (3) different male morphotypes are absent; (4) minimum sexable size and (5) minimum size of ovigerous females are smaller. These traits suggest a heterochronic shift (predisplacement) of sexual maturation and r-selection. In summary, our data show biologically relevant differences in life-history traits of shrimps from the Pantanal compared to M. amazonicum populations in other regions. All these differences persist also in long-term cultures maintained under constant conditions. Altogether, our data support the hypothesis that M amazonicum in the Paraná-Paraguay drainage basin has phylogenetically diverged from allopatric populations that are hydrologically separated by continental watersheds, implying an at least incipient vicariant speciation.

Temporal Gene Expression Variation Associated with Eyespot Size Plasticity in Bicyclus anynana

Seasonal polyphenism demonstrates an organism's ability to respond to predictable environmental variation with alternative phenotypes, each presumably better suited to its respective environment. However, the molecular mechanisms linking environmental variation to alternative phenotypes via shifts in development remain relatively unknown. Here we investigate temporal gene expression variation in the seasonally polyphenic butterfly Bicyclus anynana. This species shows drastic changes in eyespot size depending on the temperature experienced during larval development. The wet season form (larvae reared over 24°C) has large ventral wing eyespots while the dry season form (larvae reared under 19°C) has much smaller eyespots. We compared the expression of three proteins, Notch, Engrailed, and Distal-less, in the future eyespot centers of the two forms to determine if eyespot size variation is associated with heterochronic shifts in the onset of their expression. For two of these proteins, Notch and Engrailed, expression in eyespot centers occurred earlier in dry season than in wet season larvae, while Distal-less showed no temporal difference between the two forms. These results suggest that differences between dry and wet season adult wings could be due to a delay in the onset of expression of these eyespot-associated genes. Early in eyespot development, Notch and Engrailed may be functioning as repressors rather than activators of the eyespot gene network. Alternatively, temporal variation in the onset of early expressed genes between forms may have no functional consequences to eyespot size regulation and may indicate the presence of an 'hourglass' model of development in butterfly eyespots.

Statistical support for the hypothesis of developmental constraint in marsupial skull evolution

BackgroundIn contrast to placental neonates, in which all cranial bones are ossified, marsupial young have only the bones of the oral region and the exoccipital ossified at birth, in order to facilitate suckling at an early stage of development. In this study, we investigated whether this heterochronic shift in the timing of cranial ossification constrains cranial disparity in marsupials relative to placentals.MethodsWe collected three-dimensional (3D) landmark data about the crania of a wide range of extant placentals and marsupials, and from six fossil metatherians (the clade including extant marsupials and their stem relatives), using a laser scanner and a 3D digitizer. Principal components analysis and delta variance tests were used to investigate the distribution and disparity of cranial morphology between different landmark sets (optimizing either number of landmarks or number of taxa) of the whole skull and of individual developmental or functional regions (neurocranium, viscerocranium, oral region) for extant placentals and marsupials. Marsupial and placental data was also compared based on shared ecological aspects including diet, habitat, and time of peak activity.ResultsWe found that the extant marsupial taxa investigated here occupy a much smaller area of morphospace than the placental taxa, with a significantly (P<0.01) smaller overall variance. Inclusion of fossil taxa did not significantly increase the variance of metatherian cranial shape. Fossil forms generally plotted close to or within the realm of their extant marsupial relatives. When the disparities of cranial regions were investigated separately, significant differences between placentals and marsupials were seen for the viscerocranial and oral regions, but not for the neurocranial region.ConclusionThese results support the hypothesis of developmental constraint limiting the evolution of the marsupial skull, and further suggest that the marsupial viscerocranium as a whole, rather than just the early-ossifying oral region, is developmentally constrained.

Patterns and implications of extensive heterochrony in carnivoran cranial suture closure

Heterochronic changes in the rate or timing of development underpin many evolutionary transformations. In particular, the onset and rate of bone development have been the focus of many studies across large clades. In contrast, the termination of bone growth, as estimated by suture closure, has been studied far less frequently, although a few recent studies have shown this to represent a variable, although poorly understood, aspect of developmental evolution. Here, we examine suture closure patterns across 25 species of carnivoran mammals, ranging from social-insectivores to hypercarnivores, to assess variation in suture closure across taxa, identify heterochronic shifts in a phylogenetic framework and elucidate the relationship between suture closure timing and ecology. Our results show that heterochronic shifts in suture closure are widespread across Carnivora, with several shifts identified for most major clades. Carnivorans differ from patterns identified for other mammalian clades in showing high variability of palatal suture closure, no correlation between size and level of suture closure, and little phylogenetic signal outside of musteloids. Results further suggest a strong influence of feeding ecology on suture closure pattern. Most of the species with high numbers of heterochronic shifts, such as the walrus and the aardwolf, feed on invertebrates, and these taxa also showed high frequency of closure of the mandibular symphysis, a state that is relatively rare among mammals. Overall, caniforms displayed more heterochronic shifts than feliforms, suggesting that evolutionary changes in suture closure may reflect the lower diversity of cranial morphology in feliforms.

Pattern and polarity in the development and evolution of the gnathostome jaw: Both conservation and heterotopy in the branchial arches of the shark, Scyliorhinus canicula

The acquisition of jaws constitutes a landmark event in vertebrate evolution, one that in large part potentiated their success and diversification. Jaw development and patterning involves an intricate spatiotemporal series of reciprocal inductive and responsive interactions between the cephalic epithelia and the cranial neural crest (CNC) and cephalic mesodermal mesenchyme. The coordinated regulation of these interactions is critical for both the ontogenetic registration of the jaws and the evolutionary elaboration of variable jaw morphologies and designs. Current models of jaw development and evolution have been built on molecular and cellular evidence gathered mostly in amniotes such as mice, chicks and humans, and augmented by a much smaller body of work on the zebrafish. These have been partnered by essential work attempting to understand the origins of jaws that has focused on the jawless lamprey. Chondrichthyans (cartilaginous fish) are the most distant group to amniotes within extant gnathostomes, and comprise the crucial clade uniting amniotes and agnathans; yet despite their critical phylogenetic position, evidence of the molecular and cellular underpinnings of jaw development in chondrichthyans is still lacking. Recent advances in genome and molecular developmental biology of the lesser spotted dogfish shark, Scyliorhinus canicula, make it ideal for the molecular study of chondrichthyan jaw development. Here, following the ‘Hinge and Caps' model of jaw development, we have investigated evidence of heterotopic (relative changes in position) and heterochronic (relative changes in timing) shifts in gene expression, relative to amniotes, in the jaw primordia of S. canicula embryos. We demonstrate the presence of clear proximo-distal polarity in gene expression patterns in the shark embryo, thus establishing a baseline molecular baüplan for branchial arch-derived jaw development and further validating the utility of the ‘Hinge and Caps’ model in comparative studies of jaw development and evolution. Moreover, we correlate gene expression patterns with the absence of a lambdoidal junction (formed where the maxillary first arch meets the frontonasal processes) in chondrichthyans, further highlighting the importance of this region for the development and evolution of jaw structure in advanced gnathostomes.

Heterochrony and limb form variation in crested newts

AbstractThe crested newt superspecies includes four morphotypes, each characterized by a specific body‐to‐limb conformation associated with their respective ecologies: newts with large, stocky bodies and robust limbs are more terrestrial, whereas newts with small, elongate bodies and small limbs are more aquatic. This study investigated whether heterochronic transformations can account for limb form variation in light of phylogenetic history and ecology. Ossification sequence analyses revealed some synapomorphic heterochronic shifts specific to crested newts, including delay of the ossification in the second finger and accelerations in metacarpal III and metatarsal V. These shifts involve a change from pre‐axial to post‐axial dominance in a developmental sequence uncommon to caudate salamanders. No adaptive explanation of these shifts is apparent. The allometric trajectories of crested newt species were similar after metamorphosis; however, pre‐metamorphic growth showed species differences, potentially reflecting differences among species in ecological or functional demands.

The Continuing Debate on Deep Molluscan Phylogeny: Evidence for Serialia (Mollusca, Monoplacophora + Polyplacophora)

Molluscs are a diverse animal phylum with a formidable fossil record. Although there is little doubt about the monophyly of the eight extant classes, relationships between these groups are controversial. We analysed a comprehensive multilocus molecular data set for molluscs, the first to include multiple species from all classes, including five monoplacophorans in both extant families. Our analyses of five markers resolve two major clades: the first includes gastropods and bivalves sister to Serialia (monoplacophorans and chitons), and the second comprises scaphopods sister to aplacophorans and cephalopods. Traditional groupings such as Testaria, Aculifera, and Conchifera are rejected by our data with significant Approximately Unbiased (AU) test values. A new molecular clock indicates that molluscs had a terminal Precambrian origin with rapid divergence of all eight extant classes in the Cambrian. The recovery of Serialia as a derived, Late Cambrian clade is potentially in line with the stratigraphic chronology of morphologically heterogeneous early mollusc fossils. Serialia is in conflict with traditional molluscan classifications and recent phylogenomic data. Yet our hypothesis, as others from molecular data, implies frequent molluscan shell and body transformations by heterochronic shifts in development and multiple convergent adaptations, leading to the variable shells and body plans in extant lineages.

Heterochronic shifts in the ossification sequences of surface- and subsurface-dwelling skinks are correlated with the degree of limb reduction

Scincid lizards exhibit a variety of limb anatomies which reflect the functional requirements of different modes of life. Besides surface dwellers which show neither body elongation nor limb reduction, there are numerous examples that can be arranged as increasingly serpentiform taxa moving in sand, humus or leaf litter. We explored the question of whether limb reduction and body elongation in skinks are linked to heterochronic shifts in the ossification sequences. The study material comprises skinks showing four different morphotypes: Liopholis whitii, Lerista bougainvillii, Hemiergis peronii and Saiphos equalis. Results showed that (i) scincid lizards with limb reductions exhibit an earlier onset of ossification in the cervical vertebrae, and (ii) ossification starts earlier in the pectoral girdle (scapula and coracoid) and pelvic girdle (ilium, ischium and pubis) relative to the timing of the onset in elements of the forelimbs and hind limbs. Furthermore, they show (iii) an earlier strengthening of the premaxilla, which first completes the anterior part of the dorsal cranial roof, and (iv) an earlier onset of ossification in the forelimb elements than in the equivalent elements of the hind limbs. The species showing the least limb reduction (L. bougainvillii) had the greatest developmental similarity to the normally proportioned surface-dwelling species (L. whitii). S. equalis, as the morphotype with the greatest deviation from the normally proportioned, pentadactyle form, varies the most from L. whitii. The heterochronic shifts in the ossification sequences are linked to a shift in the emphasis from limbed locomotion to trunk locomotion in the species with body elongation and/or limb reduction.

Ossification sequences and associated ontogenetic changes in the bone histology of pachypleurosaurids from Monte San Giorgio (Switzerland/Italy)

ABSTRACT Evolutionary changes in lifestyle (e.g., terrestrial vs. aquatic habits) influence tetrapod limb morphology. Similar evolutionary trends in osteogenetic sequences (order of bone ossification) and bone microstructure are often shared in extant tetrapods with similar habit preferences: such data are sometimes available from extinct taxa. The pachypleurosaurids from Monte San Giorgio (Switzerland, Italy) are Triassic marine reptiles with high quality, complete ontogenetic series. We studied osteogenesis and bone histology in the four species from this locality, comparing these with data from Recent terrestrial lizards and secondarily aquatic reptiles in order to determine if the osteogenetic sequences of pachypleurosaurids were similar to either the hypothesized plesiomorphic condition for terrestrial eureptilians or those of Recent aquatic reptiles. Pachypleurosaurian limb osteogenesis occurs in two steps: (1) developmental sequences of ossification during embryology and/or in early neonates, (2a) additional primary periosteal compaction processes, and (2b) additional primary and secondary endosteal compaction processes during neonate ontogeny. Taphonomic patterns reveal information on the order of the initiation and termination of these steps, which are (A) onset of ossification, (B) onset of additional compaction processes (early phase), and (C) termination of additional compaction processes (final phase). An event pairing analysis found that ossification of forelimb elements in pachypleurosaurids precedes that of the hind limb elements in all osteogenetic stages except for initiation of ossification (A). The order of their early phase compaction processes is similar to the hypothesized plesiomorphic eureptilian condition, whereas their final phase compaction processes varies among pachypleurosaurids, with S. mirigiolensis showing minor heterochronic shifts and N. edwardsii showing many heterochronic shifts relative to the hypothesized ancestral condition. Pachypleurosaurids from Monte San Giorgio increase the number of heterochronic shifts with decreasing stratigraphic age, showing a transition from more ‘terrestrial’ to more ‘aquatic’ osteogenetic sequences in comparison to data on ossification sequences of Recent aquatic reptiles.

†Caruso, a new genus of anglerfishes from the Eocene of Monte Bolca, Italy, with a comparative osteology and phylogeny of the teleost family Lophiidae

†Caruso, a new genus of lophiid anglerfishes, erected to contain †Lophius brachysomus Agassiz from the Eocene of Monte Bolca, Italy, is described and compared osteologically with all known representatives of the family, both extinct and extant. Together with †Sharfia, known from a single specimen also from Monte Bolca, †Caruso is the oldest member of the teleost family Lophiidae known to date, based on articulated skeletal remains. It possesses several autapomorphic features as well as a unique combination of character states that clearly separate it from all other known lophiiform fishes. Evidence is provided to show that †Sharfia is the sister group of all other known lophiid taxa, that †Caruso is most closely related phylogenetically to the extant genus Sladenia, and that these two genera together form the sister group of all remaining members of the family. †Caruso brachysomus is the third valid extinct taxon of the Lophiidae known from articulated skeletal remains. Candidate developmental mechanisms that may have contributed to the origin of the lophiiform body plan are also suggested. The hypertrophic development of the jaws, suspensorium, hyoid apparatus and branchial arches typical of lophiiforms may be correlated, possibly under the influence of discrete sets of genes. The synapomorphic elongation of the pectoral-fin radials might be related to a heterochronic shift of the onset of the expression of the gene sonic hedgehog. Finally, the highly modified spinous dorsal fin may have arisen by submodularization and co-option of the first dorsal-fin module, whereas its forward shift over the neurocranium may represent an anterior shift of the stripes of competency for dorsal-fin formation along the dorsal midline.

Rate of meristem maturation determines inflorescence architecture in tomato

Flower production and crop yields are highly influenced by the architectures of inflorescences. In the compound inflorescences of tomato and related nightshades (Solanaceae), new lateral inflorescence branches develop on the flanks of older branches that have terminated in flowers through a program of plant growth known as "sympodial." Variability in the number and organization of sympodial branches produces a remarkable array of inflorescence architectures, but little is known about the mechanisms underlying sympodial growth and branching diversity. One hypothesis is that the rate of termination modulates branching. By performing deep sequencing of transcriptomes, we have captured gene expression dynamics from individual shoot meristems in tomato as they gradually transition from a vegetative state to a terminal flower. Surprisingly, we find thousands of age-dependent expression changes, even when there is little change in meristem morphology. From these data, we reveal that meristem maturation is an extremely gradual process defined molecularly by a "meristem maturation clock." Using hundreds of stage-enriched marker genes that compose this clock, we show that extreme branching, conditioned by loss of expression of the COMPOUND INFLORESCENCE gene, is driven by delaying the maturation of both apical and lateral meristems. In contrast, we find that wild tomato species display a delayed maturation only in apical meristems, which leads to modest branching. Our systems genetics approach reveals that the program for inflorescence branching is initiated surprisingly early during meristem maturation and that evolutionary diversity in inflorescence architecture is modulated by heterochronic shifts in the acquisition of floral fate.

Skeletal ossification and sequence heterochrony in xenarthran evolution

Previous analyses of how mammals vary in their ossification sequences have focused on monotremes, marsupials, and boreoeutherian placentals. Here, we focus on the sequence of cranial and postcranial ossification events during growth in the xenarthran skull and skeleton, including armadillos, anteaters, and sloths. We use two different methods to quantify sequence heterochrony: sequence analysis of variance (ANOVA) and event-paring/Parsimov. Our results indicate that Parsimov is conservative and does not detect clear heterochronic shifts between xenarthran and boreoeutherian placentals. Sequence-ANOVA performs better, but both methods exhibit sensitivity to the artifactual accumulation of ties. By controlling for ties and taking into account results that the methods have in common, our analysis suggests that xenarthrans significantly differ from other placentals by a late ossification of the sternum and an early ossification of the phalanges and pubis. We interpret these differences as showing that heterochrony plays a role in the skeletal development of xenarthrans, a change from previous studies that have emphasized the developmental homogeneity of the skeleton across placental mammals.

Evolutionary origin of a novel gene expression pattern through co-option of the latent activities of existing regulatory sequences.

Spatiotemporal changes in gene expression underlie many evolutionary novelties in nature. However, the evolutionary origins of novel expression patterns, and the transcriptional control elements ("enhancers") that govern them, remain unclear. Here, we sought to explore the molecular genetic mechanisms by which new enhancers arise. We undertook a survey of closely related Drosophila species to identify recently evolved novel gene expression patterns and traced their evolutionary history. Analyses of gene expression in a variety of developing tissues of the Drosophila melanogaster species subgroup revealed high rates of expression pattern divergence, including numerous evolutionary losses, heterochronic shifts, and expansions or contractions of expression domains. However, gains of novel expression patterns were much less frequent. One gain was observed for the Neprilysin-1 (Nep1) gene, which has evolved a unique expression pattern in optic lobe neuroblasts of Drosophila santomea. Dissection of the Nep1 cis-regulatory region localized a newly derived optic lobe enhancer activity to a region of an intron that has accumulated a small number of mutations. The Nep1 optic lobe enhancer overlaps with other enhancer activities, from which the novel activity was co-opted. We suggest that the novel optic lobe enhancer evolved by exploiting the cryptic activity of extant regulatory sequences, and this may reflect a general mechanism whereby new enhancers evolve.

New evidence for the role of heterochrony in the repeated evolution of cichlid opsin expression

SUMMARY Lake Malawi (LM) cichlids have undergone heterochronic shifts in the expression of their cone opsin genes, the genes responsible for color vision. These shifts have generated species with short-, middle-, and long-wavelength-sensitive cone photoreceptors and visual systems. However, it is unclear when during the evolution of African cichlids these shifts occurred, or whether they could account for similar short- and middle-wavelength-sensitive profiles among unrelated cichlids in Lake Tanganyika (LT). To address these questions, we surveyed opsin expression in developing fry of two African cichlids, Astatotilapia burtoni from LT and Melanochromis auratus from LM. We found that A. burtoni expresses a series of three different single-cone opsins over the course of development, while M. auratus exhibits variation in the expression of only two. Neither A. burtoni nor M. auratus exhibits much variation in the expression of its double-cone opsins. These patterns reveal that A. burtoni exhibits progressive development in the sensitivity of its single-cone photoreceptors, but direct development in the sensitivity of its double-cone photoreceptors. M. auratus exhibits neotenic development in the sensitivity of both photoreceptor sets. Given the intermediate phylogenetic placement of A. burtoni between cichlids from LT and LM, our results suggest that the ancestor of LM's cichlids exhibited a progressive developmental pattern of opsin expression. These results indicate that the heterochronic shifts which produced the short- and middle-wavelength-sensitive profiles of LM's cichlids occurred recently, and suggest that the presence of similar profiles among LT's cichlids are due to parallel heterochronic shifts.

Developmental transformations in Jurassic driftwood crinoids

The internal, multi-element skeleton of echinoderms can differentiate almost as much as that of the vertebrates. The implied probability of post-mortem disarticulation was bypassed in pelagic species, whose carcasses could sink directly onto toxic sea bottoms. Among them were isocrinids attached to driftwood. In the Toarcian Posidonia Shales they are represented by two easily distinguishable forms: (1) the giant and long-stemmed Seirocrinus was probably a passive tow-net filtrator; (2) the smaller and heavily cirrated Pentacrinites may have produced its own filter current, even though this assumption is in conflict with the distribution of muscles in present-day benthic Isocrinida. In a newly discovered colony of the smaller Early Liassic Pentacrinites fossilis, both strategies are found together. This leads to the hypothesis that the two Toarcian forms may also represent developmental stages of the same species. After the Toarcian, Seirocrinus (as either a taxon or a developmental stage) became extinct, probably due to shipworms reducing the drifting time of logs. In contrast, the proposed feeding style of Pentacrinites allowed it to return to the benthic realm, but in an inverted attitude. During this complex history, most adaptational changes required only heterochronic shifts in the development of tegmen, arms, pinnules, stem, and cirri. Unrelated pseudoplanktonic crinoids of earlier times show convergent adaptations with different pathways.

Imaging of Transgenic Cricket Embryos Reveals Cell Movements Consistent with a Syncytial Patterning Mechanism

The mode of insect embryogenesis varies among species, reflecting adaptations to different life history strategies [1, 2]. In holometabolous insects, which include the model systems, such as the fruit fly and the red flour beetle, a large proportion of the blastoderm produces an embryo, whereas hemimetabolous embryos generally arise from a small region of the blastoderm [3]. Despite their importance in evolutionary studies, information of early developmental dynamics of hemimetabolous insects remains limited. Here, to clarify how maternal and gap gene products act in patterning the embryo of basal hemimetabolous insects, we analyzed the dynamic segmentation process in transgenic embryos of an intermediate-germ insect species, the cricket, Gryllus bimaculatus. Our data based on live imaging of fluorescently labeled embryonic cells and nuclei suggest that the positional specification of the cellular blastoderm may be established in the syncytium, where maternally derived gradients could act fundamentally in a way that is similar to that of Drosophila, namely throughout the egg. Then, the blastoderm cells move dynamically, retaining their positional information to form the posteriorly localized germ anlage. Furthermore, we find that the anterior head region of the cricket embryo is specified by orthodenticle in a cellular environment earlier than the gnathal and thoracic regions. Our findings imply that the syncytial mode of the early segmentation in long-germ insects evolved from a dynamic syncytial-to-cellular mode found in the present study, accompanied by a heterochronic shift of gap gene action.

Heterochrony of cranial features associated with wide jaw gapes in common marmosets (Callithrix jacchus)

Marmosets are unique among platyrrhines for habitually gouging trees with their anterior teeth to stimulate exudate flow. We previously demonstrated that marmosets exhibit cranial features that facilitate biting at wide jaw gapes during gouging, as compared to skulls of non‐gouging tamarins. Here we examine the role of heterochronic shifts during the ontogeny of cranial features facilitating wide gapes.Three cranial dimensions associated with wide gapes were measured, as well as three dimensions related to load resistance in ontogenetic series from neonates to adults of marmosets (Callithrix jacchus, N=129) and tamarins (Saguinus fuscicollis, N=135). All specimens were captive individuals housed at Oak Ridge Associated Universities' Colony with known ages at death.Marmosets exhibit a complex pattern of heterochronic shifts in cranial features linked to wide gape throughout ontogeny relative to tamarins. The relatively elongated anteroposterior glenoid, condyle and mandible of marmosets consistently appear peramorphic during ontogeny. Corporal and symphyseal dimensions associated with load resistance consistently appear paedomorphic in marmosets.Results support a hypothesis that the shape differences facilitating wide jaw gapes are the result of multiple heterochronic shifts in ontogenetic trajectories between gouging marmosets and non‐gouging tamarins.Supported by NSF (BCS‐0412153, BCS‐0094666).Grant Funding Source: Supported by NSF (BCS‐0412153, BCS‐0094666)