Ontogeny and phylogeny: a quantitative theory of heterochrony

Developmental variability in organisms underlies the relationship between ontogeny and phylogeny. The concept entropy permits a quantitative characterization of this variability and provides a basis for interpreting the phylogeny of heterochrony in evolution.     

Ontogeny and phylogeny in temnospondyls: a new method of analysis

A new method has been devised to compare the ontogeny and phylogeny of some of the better documented tetrapods from the Stephanian to the Trias. This approach is based on global parsimony analysis of several temnospondyl amphibians, in which some ontogenetic sequences have been highlighted. Forty-one homologous morphoanatomical character states have been separated into larval, juvenile and adult stages of each of six tetrapod species. The taxonomic congruence (TC) approach involves comparing trees based on larval, juvenile and adult character states. These so-called 'ontotrees' are not congruent, either in their topologies or in the distribution of the character states. The total evidence (TE) approach involves a combined analysis of all the character states observed in the various growth stages of the taxa, and is secondarily used in order to test this taxonomic incongruence. In this case, the TE result corroborates the TC analysis: the TE tree is robust and reveals a few homoplasies which cause the taxonomic incongruence. This is interpreted as either the result of heterochronic events in temnospondyl evolution, or as the product of inaccurate identification of larval and metamorphic fossil forms.     

Ontogeny and phylogeny in papionin primates

This study investigates the developmental bases of size and shape variation in papionin primates (Macaca, Cercocebus, Mandrillus, Lophocebus, and Papio). The analysis tests hypotheses predicting that heterochronic changes in ontogeny, particularly in the degree of overall size growth, can account for cranial diversity and "allometric scaling" in this clade. Large developmental samples of extant papionin crania are examined to test heterochronic hypotheses using bivariate allometric methods. Analyses indicate that the crania of larger papionins (Mandrillus and Papio) are generally peramorphic, surpassing size and shape ranges of smaller, and probably less-derived, macaques and mangabeys. At least two heterochronic processes, including acceleration and hypermorphosis, can account for this pattern. Ontogenetic changes include decoupling of growth and development among cranial regions, along with simple shifts in size. Allometric scaling has complex developmental bases. Size change itself is not sufficient to explain all developmental differences among papionins, but these changes are extremely important in comparisons within cranial regions such as the face. Results imply that Papio exhibits strongly derived patterns of brain growth that impact postnatal patterns of size and shape transformation. Consideration of these results in the context of recent socioecological analyses suggests that derived patterns of cranial growth in Papio may be a response to selection during the early periods of ontogeny, resulting in a distinctive life history pattern.     

Ontogeny tends to recapitulate phylogeny in digital organisms

Abstract Biologists have long debated whether ontogeny recapitulates phylogeny and, if so, why. Two plausible explanations are that (i) changes to early developmental stages are selected against because they tend to disrupt later development and (ii) simpler structures often precede more complex ones in both ontogeny and phylogeny if the former serve as building blocks for the latter. It is difficult to test these hypotheses experimentally in natural systems, so we used a computational system that exhibits evolutionary dynamics. We observed that ontogeny does indeed recapitulate phylogeny; traits that arose earlier in a lineage's history also tended to be expressed earlier in the development of individuals. The relative complexity of traits contributed substantially to this correlation, but a significant tendency toward recapitulation remained even after accounting for trait complexity. This additional effect provides evidence that selection against developmental disruption also contributed to the conservation of early stages in development.     

Ontogeny discombobulates phylogeny: paedomorphosis and higher-level salamander relationships

Evolutionary developmental biology ("evo-devo") has revolutionized evolutionary biology but has had relatively little impact on systematics. We show that similar large-scale developmental changes in distantly related lineages can dramatically mislead phylogenetic analyses based on morphological data. Salamanders are important model systems in many fields of biology and are of special interest in that many species are paedomorphic and thus never complete metamorphosis. A recent study of higher-level salamander phylogeny placed most paedomorphic families in a single clade based on morphological data. Here, we use new molecular and morphological data to show that this result most likely was caused by the misleading effects of paedomorphosis. We also provide a well-supported estimate of higher-level salamander relationships based on combined molecular and morphological data. Many authors have suggested that paedomorphosis may be problematic in studies of salamander phylogeny, but this hypothesis has never been tested with a rigorous phylogenetic analysis. We find that the misleading effects of paedomorphosis on phylogenetic analysis go beyond the sharing of homoplastic larval traits by paedomorphic adults, and the problem therefore is not solved by simply excluding suspected paedomorphic characters. Instead, two additional factors are critically important in causing paedomorphic species to be phylogenetically "misplaced": (1) the absence of clade-specific synapomorphies that develop during metamorphosis in nonpaedomorphic taxa and allow their "correct" placement and (2) parallel adaptive changes associated with the aquatic habitat of the larval stage. Our results suggest that the effects of paedomorphosis on phylogenetic analyses may be complex, difficult to detect, and can lead to results that are both wrong and statistically well supported by parsimony and Bayesian analyses.     

Ontogeny and phylogeny in the evolutionary biochemistry space

The process of evolution is considered as the change of nucleotide sequence in an (N+1)-dimensional or 3-dimensional space. Restricting conditions may be represented by the shape of a tunnel, through which points or a rope representing nucleic acids move along with time, and may be similar for ontogenetic and phylogenetic development.     

Ontogeny and phylogeny in the evolutionary biochemistry space

The process of evolution is considered as the change of nucleotide sequence in an (N+1)-dimensional or 3-dimensional space. Restricting conditions may be represented by the shape of a tunnel, through which points or a rope representing nucleic acids move along with time, and may be similar for ontogenetic and phylogenetic development.     

Ontogeny and phylogeny of Brownleea (Orchidoideae: Orchidaceae)

The phylogeny of the African orchidoid genus Brownleea was investigated, using morphological characters. It has been suggested that the genus may be of hybrid origin, a hypothesis supported by the presence of two very different types of stigma ontogenies. Morphological investigations of all the species revealed that two species have stigmas derived from all three carpel apices, the 'normal' situation in the Orchidaceae. The remaining five species have stigmas derived from only the median carpel, a very unusual situation found in the Coryciinae. A phylogenetic analysis of all available morphological data for all species supports the monophyly of the genus. based on several distinct synapomorphies. The variation in stigma ontogeny may be due either to parallelism, or to an earlier hybridization event. The analysis supported the recognition of several distinct groupings within Brownleea . Two of these groupings are supported irrespective of which putative parent is used as sister-group to the genus, while a third grouping is dependent on the use of the as sister-group.     

Ontogeny and phylogeny of tooth attachment modes in actinopterygian fishes

There are four major tooth attachment modes in actinopterygians. Type 1 mode is characterized by complete ankylosis of the tooth to the attachment bone; it is the primitive attachment mode for actinopterygians. In Type 2 mode there is a ring of collagen between the tooth base and the bone. In Type 3 mode mineralization extends near or to the bone at the anterior tooth border, and there is a relatively large collagen area on the posterior surface of the tooth; Type 3 teeth are hinged with an anterior axis of rotation. Type 4 teeth also have a relatively large posterior collagen area, but there is no collagenous connection between the anterior basal tooth border and the attachment bone; Type 4 teeth are hinged, with a posterior axis of rotation. Types 2, 3, and 4 attachment modes appear to result from retardation of mineralization and resemble, with some modifications, ontogenetic stages in the development of Type 1 mode; they are considered to be paedomorphic features. Attachment modes 2, 3, and 4 are each associated with a major evolutionary lineage within the Teleostei. The degree to which paedomorphosis has been a factor in teleostean evolution is discussed.     

Ontogeny and phylogeny of endothermy and torpor in mammals and birds

Endothermic thermoregulation in small, altricial mammals and birds develops at about one third to half of adult size. The small size and consequently high heat loss in these young should result in more pronounced energetic challenges than in adults. Thus, employing torpor (a controlled reduction of metabolic rate and body temperature) during development would allow them to save energy. Although torpor during development in endotherms is likely to occur in many species, it has been documented in only a few. In small, altricial birds (4 orders) and marsupials (1 order), which are poikilothermic at hatching/birth, the development of competent endothermic thermoregulation during cold exposure appears to be concurrent with the capability to display torpor (i.e. poikilothermy is followed by heterothermy), supporting the view that torpor is phylogenetically old and likely plesiomorphic. In contrast, in small, altricial placental mammals (2 orders), poikilothermy at birth is followed first by a homeothermic phase after endothermic thermoregulation is established; the ability to employ torpor develops later (i.e. poikilothermy-homeothermy-heterothermy). This suggests that in placentals torpor is a derived trait that evolved secondarily after a homeothermic phase in certain taxa perhaps as a response to energetic challenges. As mammals and birds arose from different reptilian lineages, endothermy likely evolved separately in the two classes, and given that the developmental sequence of torpor differs between marsupials and placentals, torpor seems to have evolved at least thrice.     

Ontogeny and phylogeny of Upper Cenomanian rotaliporids (Foraminifera)

The fossil record of planktonic foraminifera is a key source of data on the evolution of marine plankton. One of the most distinctive groups of Cretaceous foraminifera, the rotaliporids, widely used as a stratigraphic index, has always been considered to be a monophyletic clade. New data on the coiling direction and persistent morphological features of the late rotaliporids from the Upper Cenomanian of the Western Interior Seaway, USA, and the Vocontian Basin of southeast France is used as a phylogenetic proxy. Dealing with key morphological features, the coiling pattern of these keeled morphotypes proves that the rotaliporids group is polyphyletic and composed of Thalmanninella, that displays a dextral-coiling preference, and Rotalipora s.s., that have a proportionate-coiling mode. The stratigraphically youngest rotaliporids with keels co-occur with globular forms; and all morphologies transitional between these morphotypes are observed. The ontogenetic relationships between them are investigated, indicating that loss of the keel was a selective advantage that enabled those rotaliporids to remain in the surface water, thereby avoiding the expansion of the oxygen minimum zone. Two species are observed: Thalmanninella multiloculata and Rotalipora planoconvexa. These species are interpreted as having arisen by neoteny from Thalmanninella greenhornensis and Rotalipora cushmani respectively.     

Ontogeny, phylogeny and the origin of biological information.

Accepting the evidence that evolution is largely finished and that sexual reproduction is incapable of supporting macroevolution, indicates that macroevolutionary changes were produced presexually through the cytological events associated with the first meiotic division. This reproductive mode is ideally suited to the production of new structural rearrangements of preexisting genetic information in instantaneous homozygous form. These new arrangements (position effects) produce new and discrete species. Thus, speciation results not from new genetic information, but rather from information already present (preformed). The several parallels that exist between epigenesis and preformation in both ontogeny (development) and phylogeny (evolution) are discussed. I propose that both of these phenomena have proceeded through the selective activation (derepression) of an enormous potential supply of information already present at the onset of each of these biological phenomena. Acceptance of these possibilities can serve to liberate us in our quest for the ultimate truth concerning these two closely related phenomena.     

Advances in understanding hyphal morphogenesis: Ontogeny,phylogeny and cellular localization of chitin synthases

Hyphal morphogenesis is largely determined by the mode the cell wall is synthesized. One of the main structural components of the cell wall is the chitin microfibril, whose synthesis is catalyzed at the cell surface by an organized but not fully understood complex of chitin-synthesizing enzymes. Genetic studies have identified several chitin synthase genes (chs) among different fungi. In each given species, several chitin synthases (CHS) may be present. These have been assigned to different classes (I–VII) on the basis of characteristic amino acid sequences. A revised phylogenetic scheme of fungal CHS is presented but there was no apparent correlation between CHS class and a specific cell function or cell cycle stage. The availability of methodology to make genetic fusions between CHS and green fluorescent protein (GFP) and to follow them in living cells with high-resolution confocal microscopy and widefield fluorescence microscopy has made it possible to study the location and dynamics of different CHS in several fungi. Among these, Neurospora crassa was recently used to analyse the spatial distribution and role of chitin synthases in hyphal tip growth. Here we summarise recent advances in this area with particular emphasis on N. crassa. CHS-3, CHS-6 and more recently CHS-1 are abundantly present in the distal regions of the hypha and contained in membranous structures of different shapes from spheres to elongated tubes; as the GFP–CHS tagged structures advance towards the tip, they begin to disintegrate. In the subapical region GFP–CHS was not found in large organelles; it only occurred as fine punctuate fluorescence. These minute structures are probably chitosomes. Finally, at the tip there is always a conspicuous accumulation of GFP–CHS in the Spitzenkörper core where microvesicles are known to accumulate. The collective evidence points to CHS travelling to its destination at the hyphal apex via a secretory route distinct from the conventional ER–Golgi route. The accumulation of CHS microvesicles at the Spk reinforces the view that this structure plays a pivotal role in cell wall growth and hyphal morphogenesis.     

Ontogeny and phylogeny of the trunk lateral line system in cichlid fishes

An examination of the ontogeny of the lateral line trunk canal and the diversity of adult trunk canal patterns among cichlids indicates that bidirectional canal formation is a general ontogenetic pattern in the Cichlidae with the exception of Cichla and those few species with a complete trunk canal pattern. In addition to the tubed scales which make up the trunk canal, some lateral line scales have pits containing superficial neuromasts. These are recognized as components of the lateral line system of the trunk in adult cichlids for the first time. Eight trunk canal patterns that are variations on a simple disjunct pattern are defined among the 17 cichlid genera examined. Using bidirectional canal formation as a developmental model, these patterns can be placed along an ontogenetic spectrum. This suggests that heterochrony (alterations in the timing of development) is an important mechanism of evolutionary change in the lateral line system of the trunk in cichlid fishes.     

Ontogeny and phylogeny of femoro-tibial characters in humans and hominid fossils: functional influence and genetic determinism.

Three different human femoro-tibial characters are selected as functionally relevant and derived hominid characters: femoral bicondylar angle, shape of the femoral distal epiphysis, and the tibial insertion of the lateral meniscus. The timing and mode of formation of these characters are investigated during human ontogeny and are shown to differ considerably. The available hominid fossils (Australopithecus afarensis and early Homo) are interpreted in the light of this ontogenetic analysis with the conclusion that, during hominid evolution, different modes of selection of these features must have occurred. In modern humans, the femoral bicondylar angle proves to be an epigenetic functional feature, which develops during early childhood growth. It is present in all australopithecines and we suggest that it developed following a change in their locomotor behavior and not upon a genomic change: the early practice of bipedal walking, with adducted knee joints, in the locomotor repertoire of infant australopithecines, was sufficient to promote this angle. Later in hominid evolution, the knee joint evolved from having a single insertion of the lateral meniscus on the tibia to a double one. While Australopithecus afarensis exhibits a single insertion, early Homo clearly exhibits a double insertion of the lateral meniscus on the tibia. The double insertion restricts the mobility of the meniscus on the tibial plateau, indicating a habitual practice of full extension movements of the knee joint. Among modern humans, the posterior insertion of the lateral meniscus appears early in fetal life. Consequently in early Homo, this new selected feature developed directly as a result of a genomic change. The derived shape of human distal femoral epiphysis includes a prominence of the lateral lip of the femoral trochlea, an elliptical profile of the lateral condyle, and an anteroposterior lengthening of the epiphysis. Analysis of human fetal and neonatal distal epiphyses shows that the prominence of the lateral lip of the trochlea arises before any use, and thus appears to be genetically determined. However, the postnatal development of this joint shows that this feature is also modified epigenetically by use. It is argued that the hominid femoro-patellar joint would have been reshaped following the process of genetic assimilation (Waddington [1942] Nature 3811:563-565). The prominence of the lateral lip of the femoral trochlea was probably selected following a two-staged process-first epigenetic, then genetic. Far from being a Lamarckian explanation, this concept applies precisely to adaptive characters that are induced by an external stimulus during a single lifetime and are replaced through natural selection by genetically based equivalent characters. The nature of the structures involved in the studied features is shown to be an important parameter determining their mode of development and selection.     

Ontogeny and phylogeny: molecular signatures of selection, constraint, and temporal pleiotropy in the development ofDrosophila

Background  

Karl Ernst Von Baer noted that species tend to show greater morphological divergence in later stages of development when compared to earlier stages. Darwin originally interpreted these observations via a selectionist framework, suggesting that divergence should be greatest during ontogenic stages in which organisms experienced varying 'conditions of existence' and opportunity for differential selection. Modern hypotheses have focused on the notion that genes and structures involved in early development will be under stronger purifying selection due to the deleterious pleiotropic effects of mutations propagating over the course of ontogeny, also known as the developmental constraint hypothesis.