10

 ONTOGENY:  THE  WORKSHOP  OF

  EVOLUTIONARY  CHANGE 

              

                Ontogeny does not recapitulate phylogeny: it creates it.

                                                                                                                                         W. Garstang

                                                                                                 

                                                                                                  Ontogenies evolve, not genes or adults. adults.                                                                                              M.L. McKinney and J.L. Gittleman

                                                                                                         Gittleman                               

                                                                                                     

Due to the extraordinarily complex structures and functions, metazoans, in distinction from unicellulars, cannot produce “copies of themselves”. Instead they produce unicellular entities that, themselves (egg cells) or via the union with another germ cell (sperm cell), based on the epigenetic information they are parentally provided with, are able to advance their development up to the phylotypic stage, when the embryo becomes capable of generating the information necessary for the postphylotypic development. All the evolutionary changes in metazoan morphology come into being during ontogeny, the individual development. There is no other way evolutionary changes can be actualized but via the process of ontogeny. The evolutionary changes that the species went through during its phylogeny are imprinted in the processes of individual development. The study of ontogeny, the file of inherited changes the species underwent in the course of evolution, is key to understanding the morphological evolution in metazoans.

 

Sexual reproduction is by far the predominant form of reproduction in metazoans. Parthenogenesis is a less frequent phenomenon sometimes alternated with sexual reproduction. Asexual reproduction by budding is restricted to a limited number of primitive invertebrates like Hydra.

In distinction from unicellulars which, via binary fission, produce “copies” of themselves (two daughter cells), metazoans, due to constraints imposed by the complexity of their structure cannot produce copies of themselves and produce instead unicellular structures, egg- and sperm cells, capable of independently developing into adult organisms of their kind.

While unicellulars rely for their reproduction on a template, Watson-Crick, form of heredity (the parental organism replicates itself), metazoan heredity is of a communicative type. Metazoans do not build the structure of the young but only communicate, via the gametes, epigenetic information that enables the zygote (egg cell in parthenogenetic organisms) to develop up to the phylotypic stage, when the embryo is capable of generating itself the epigenetic information for the rest of individual development.

The development of the zygote (egg cell in parthenogenetic organisms) in metazoans is enabled by deposition of the epigenetic information for the early development from the egg/zygote to the phylotypic stage. This information is provided to the gamete(s) parentally in the form of cytoplasmic factors, which control and regulate the blastula, gastrula, and neurula stages initially by their own activity and later by regulating expression of zygotic genes. In placentals, maternal factors continue to influence ontogenetic processes for the whole period of intrauterine development.

As we have shown, from an informational point of view, the process of metazoan reproduction is a biphasic and discontinuous process in which after the parentally controlled early development, the postphylotypic stage is taken over by the embryonic CNS (see chapter 7, The Epigenetic System of Heredity – An Outline).

The process of individual development from a single cell, an egg cell or a zygote, to an adult organism is known as ontogeny. From an evolutionary theoretical point of view, it represents the first laboratory for antenatally testing new developmental solutions and evolutionary changes, before they are put through the sieve of natural selection under natural conditions.

Recapitulationist followers of Ernst Haeckel (1834-1919), held that in embryonic stages of all animals we can distinguish features of their adult ancestors. Accordingly, the study of ontogeny would give biologists information for reconstructing animal phylogenies. Now, most biologists, following Karl Ernst von Baer (1792-1876), believe that only embryonic, not adult, ancestral features are that appear in the embryonic stages of animals (figure 10.1).

 

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Haeckel’s biogenetic law has been continually criticized, especially its central tenet that ontogeny recapitulates phylogeny. However, E. Mayr has warned us against a “water-bathist” approach in dealing with the law:

 

The invalidity of (Haeckel’s) law has been demonstrated so often, and so conclusively, that it is easy to fall into the opposite extreme and ignore the fact that many organisms that are highly dissimilar as adults go through similar larval stages. (Mayr, 1963b)

 

And the fact that evolutionary relationships between species and higher taxa often are reflected in similarities of early stages of their embryonic development is the reason why

 

Haeckelian concepts have survived, usually misattributed to von Baer, in the disciplines using a comparative approach to the study of morphological pattern, such as comparative anatomy, paleontology, and classical comparative embryology. These are areas where the neodarwinian “populational” approach has not influenced much the classical methodology. For example, Haeckelian concepts underlie most ontogenetic arguments utilized in the determination of homologies in comparative morphology. (Alberch and Blanco, 1996)

 

Despite the theoretical value, the almost two centuries long dispute between supporters of these opposing views has contributed little to the deeper causal question: Why must ontogeny occur at all?

One of the basic tenets of the neoDarwinian paradigm is that zygote is in possession of the whole amount of genetic information necessary for the development of the adult organism. If one would follow this still prevailing view, the conservation of the phylotypic stage and repetition of some embryonic stages in species standing higher on the tree of evolution, would evolutionarily make no sense. Logically, the question would arise: If the genetic information or the so-called genetic program for developing the species-specific structure is present in gamete(s) from the beginning, why has the embryo to follow that circuitous and very costly path often involving development of structures that are apoptotically eliminated later in the individual development? This is not the way evolution works. Evolution would have done away with the costly building of ancestral embryonic structures that have to be repeatedly replaced or transformed.

The cost of developing embryonic structures that later are apoptotically lost, is so high that were they unnecessary or “vestigial” biological phenomena, strong evolutionary pressures would have arisen for not building them at all. When this is considered in the context of the universal occurrence of that ontogenetic “replay” of embryonic features in Animalia, it would be quite logical to believe that the “recapitulation” has functions, which outweigh its excessive biological cost.

According to the epigenetic view developed in this work, the circuitous character of ontogeny is imposed by the fact that metazoan egg/zygote is not in possession of all the information necessary for the individual development. As shown earlier, the egg cell/zygote is only provided with information necessary for the early development, until the phylotypic stage. All the species of a phylum starting from different situations converge to a common parentally-determined Bauplan at the phylotypic stage. At this juncture, the function of the parental epigenetic information has terminated and the post-phylotypic development is taken over by the embryonic CNS. The epigenetic information for developing the species-specific structure is generated step-wise in a sequential process, where the embryonic structure of one stage is used for computating the epigenetic information for the next stage, by the CNS, based on its “self-organizing properties” and its close interaction with the whole embryonic structure.

 

Ontogeny and the Phylotypic Stage - Why Do All Developmental Pathways Converge to the Common Bauplan?

 

The development of vertebrate embryos starts with the zygote going through a few intermediate stages (blastula, gastrula, neurula) before reaching the phylotypic stage, when embryos of different species, which heretofore may display distinct morphologies, converge to the common Bauplan of the phylum known as pharyngula, identified by William Ballard as essentially “an early post-neurula “larva” with paired pharyngeal slits and initiation of the basic vertebrate organ systems”. Pharyngula is in possession of the dorsal nerve cord, notochord, pharyngeal arches, somites, and the tail. A similar stage of embryonic development, when all the species converge to a common Bauplan, is also observed in most invertebrates. In arthropods it is known as segmented germ band, which also appears after gastrulation.

The phylotypic stage is a watershed in the individual development from the point of view of the source of information. At this point in time the parental epigenetic information, i.e. parental mRNAs, proteins, hormones, neurotransmitters, nutrients, and other parental chemicals provided via gametes in the form of cytoplasmic factors, is totally consumed or no longer functional. This moment of “informational crisis”, coincides with the beginning of the accelerated process of development characterized by numerous inductions of neural origin leading to complex processes of cell differentiation, histogenesis and organogenesis, which require huge and ever-increasing amounts of information. Exactly at this moment, at the phylotypic stage (whether it is a vertebrate pharyngula, an insect segmented germ band, or an annelid “segmented germ band”), the embryo has succeeded in developing a CNS that is anatomically formed and physiologically ready to control the further embryonic development. It takes over the individual development up to adulthood.

In defining the vertebrate phylotypic stage, W. Ballard points out:

 

The pharyngula exhibits the basic anatomical pattern of all vetebrates in its simplest form: a set of similar organs, similarly arranged with respect to a bilaterally symmetrical body axis, possessing chiefly the characters that are common to all the vertebrate classes…One sees in them [the pharyngulas of vertebrates] epidermis but no scales, hair or feathers; kidney tubules and longitudinal kidney ducts are there, but no metanephros; all the little hearts have the same four chambers and there is at least a transient cloaca; there are no middle ears, no gills on the pharynx segments, no tongue, penis, uterus, etc. Basically just vertebrate anatomy, unobscured by the vast array of characters that appear later in development to distinguish the various classes, orders, and families. (Ballard, 1981)

 

Recently, the conventional concept of the phylotypic stage has been criticized by a number of authors. Based on a  review of the pertinent  evidence, Richardson et al. believe that it is inappropriate even to talk about a phylotypic stage, which reflects Haeckel’s inaccurate views on ontogeny as recapitulation of phylogeny. What he proposes instead is a concept of  “a phylotypic “period”” because this avoids the idea of a narrow timepoint implied by the word “stage”” (Richardson, 1995). However, from a semantic aspect, his critique is hardly justified for commonly in dictionaries of the English the word “stage” defines not a moment or point in time but a period of time the word stage is explained as “one step or degree in a process; period of development”, and the word period as “a portion of time having certain features or conditions”  (The World Book Dictionary, 1971). A number of other authors agree with Richardson. For example, Schmidt and Starck, while identifying for the zebrafish “a period of restricted variation of the phenotype due to internal developmental constraints” add that “there is no highly conserved embryonic stage in vertebrate embryos but rather a period of general similarity” (Schmidt and Starck, 2004). Even from this quantitative aspect (conserved vs. highly conserved) the proposed change is  not easier to be argued.

I find convincing Hall’s argument that:

 

Ballard’s phylotypic stage is essentially a visceral animal - head, branchial arches, bilateral symmetrical organs. His criteria were presence of somites, a neural tube: ‘Basically just vertebrate anatomy, unobscured by the vast array of characters that appear later in development’. Richardson et al. focus on features such as size, numbers of somites, presence or absence of fin or limb buds, types of neurulation, and time of appearance of structures. Their rejection of the phylotypic stage therefore, is not based on criteria used by Ballard to define the stage. The features they emphasize are, in large part, embryonic, larval, or life history adaptations. Arriving at conserved stages by different mechanisms or with different numbers of repeated units is not a reason for negating the existence of the stages. Rather, temporal variability in appearance of conserved characters directs us to seek the phylogenetic suite of characters that typifies a taxon: to ask why those characters so often appear at a conserved phylotypic stage: and to understand which developmental and evolutionary processes regulate the temporal and spatial appearance of those characters. (Hall, 1997).

 

von Baer’s laws say that the development of vertebrate embryos proceeds from general features, which are shared by all of them, to more specific features. In other words, the laws predict that the earliest embryonic stages must be uniform. However, numerous exceptions are known (Hall, 1998d) when, starting from different initial states, embryos of different taxa of the same phylum converge to the morphologically common type, the Bauplan of the phylum. So, e.g., the hylid frogs of the genus Gastrotheca display a pattern of gastrulation from an embryonic disc and an egg size that are typical of birds, not of amphibians. But this does affect neither the Bauplan nor the adult frog morphology. Pre-phylotypic stage modifications of developmental patterns that do not affect the adult morphology are also observed in taxa which were subject to modification or even to elimination of their larval structure. So, e.g., a species developing via a complex feeding larva and its congener, which develops directly, have different embryonic cell lineages and divergent patterns of early development, but converge on the adult sea urchin body plan (Raff, 1998).

The morphoconvergent phase is followed by a morphodivergent phase after the phylotypic stage with a clear tendency toward divergent types of species-specific morphologies (figure 10.2).

 

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The phylotypic stage is characterized by inductions initiated by the neural tube/CNS. These inductions lead to global interactions with the target tissues that are observed during the phylotypic stage, which narrow the field of the possibilities of evolutionary changes. Constraints imposed on the evolutionary changes during this stage are best illustrated by the conservation of the structure of organs (the number of digits and bones in amniotes and of cervical vertebrae in mammals, e.g.) that are determined during the phylotypic stage. Not only is the phylotypic stage itself a conserved stage but the organs that develop during that stage also are refractory to evolutionary change (Galis et al., 2001).

Why do metazoan embryos converge to a common Bauplan before they start developing class-, order- and species-specific features? As of yet, modern biology has no firm or convincing answer to this question.

In attempting to understand the developmental significance of the phylotypic stage one should start by examining the spatio-temporal pattern of events associated with the stage. The formation of the Bauplan of the phylum at that stage coincides with two crucial events, which are:

Firstly, termination of the function of the epigenetic information, i.e. the parental cytoplasmic factors, and

Secondly, the development of the embryonic CNS, which at this stage is operational and triggers a series of inductive events.

The systematic correlation of these three events (the Bauplan, exhaustion of parental epigenetic information and the formation of the operative embryonic CNS) in the early vertebrate ontogeny suggests that a causal relationship between them might exist.

We may reasonably relate the two last events to each other for both represent sequential and complementary sources of epigenetic information necessary, respectively, for pre- and postphylotypic development. The fact that the exhaustion of parentally provided epigenetic information coincides with the formation of the operational CNS is unlikely to be a mere coincidence for vast evidence shows that the CNS starts a series of inductions exactly when the reserve of epigenetic information is exhausted.

But may we relate the appearance of the Bauplan to the function of the embryonic CNS? The coincidence of the formation of the Bauplan with formation of the operational CNS at the phylotypic stage would suggest that this rudimentary phylotypic outline of the future organism may be necessary for the CNS as a preparatory groundwork and as a point of reference for the future direction of the individual development.

My hypothesis is that the Bauplan serves as developmental outline of the phylum that the embryonic CNS requires for fashioning initial patterns of synaptic connections and neural circuitries as its functional information-generating units. Additionally the Bauplan may provide the CNS with a general sense of direction for the post-phylotypic development.

The common phylotypic structure (Bauplan of the phylum), on the one hand, and the specificity of the incipient operational CNS at that stage, on the other, determine the divergent species-specific paths of post-phylotypic development. As we have shown earlier, it is the CNS that determines the development of the post-phylotypic embryonic structure by starting a series of global and local inductions. The structure, function, and properties of neural circuits change in response to the changing input on the developing embryonic structure.

By continually interacting with the developing embryonic structure, the CNS is able, in a self-sustainable mode, to generate stage-specific epigenetic information for the sequential stages of the post-phylotypic development up to adulthood. The fact that the CNS is not in possession of information for the post-phylotypic development, but has to generate it in a process of “learning”, by processing the input from the developing embryonic structure may be the cause of the circuitous character of ontogenetic processes.

Alternatively, it is possible that the evolutionary disadvantage of the “recapitulation” during the ontogeny of the embryonic ancestral structures has been overcompensated by the another evolutionary advantage. The “recapitulated” embryonic structures, may not be mere remnants of the phylogeny; they may serve Animalia to “memorize” lost ancestral features and the respective developmental programs. The conservation of developmental programs for these structures is neither a biological luxury nor designed to help us reconstruct phylogenies. It may be a potential adaptive mechanism worthy its high biological cost. It may be a repository of lost ancestral developmental programs that metazoans may retrieve in a “rainy day”, when the environment changes in direction of ancestral or quasi-ancestral conditions. Vast evidence on evolutionary reversions (see chapter 16 Evolution by Reverting to Ancestral Characters) may represent a validation of the hypothesis.

Many changes in morphology during the evolution of Animalia are related to drastic changes in the environment, such as transitions from a type of environment to another (terrestrial-aquatic, aquatic surface to bottom dwelling, seashore to open sea, low to high altitudes above the sea level, forest to prairies, cold, moderate, or warm climates, etc.).

It is not a rare occurrence that species in the course of evolution suddenly find themselves in very different or even contrasting habitats that may happen to be similar to those inhabited by their evolutionary ancestors. Under such drastically changed conditions, species survival would be in danger if individual organisms would not be able to rapidly (in evolutionary “instants”) adapt their behavior, morphology, and physiology to the changed conditions of life. Under such circumstances, there is no time for gradual, long term evolutionary adaptation in nature; under such circumstances, the neoDarwinian paradigm, in all its variants, sees no solution but unavoidable extinction of species. In order for the species to survive, under such circumstances, there is no alternative but sudden morphological, physiological, and/or behavioral adaptation to the changed conditions. At such junctures the ontogenetic retrieval and replay of ancestral structures during the individual development may offer off-the shelf solutions for rapid adaptation.

It is impossible to prove now that this is what has occurred in the cases of evolutionary reversions, but we have adequate corroborating evidence that metazoans, in response to stressful changes in environment, can switch to alternative and ancestral developmental pathways and life histories (see chapters 12 and 16 on transgenerational plasticity and evolutionary reversions, respectively).

Based on this ability to retrieve and replay ancestral epigenetic programs during ontogeny some salamanders switch to ancestral modes of  individual development, by entering  metamorphosis or avoiding it, depending on the conditions in the habitat. Based on this ability metazoans have so frequently reverted to ancestral morphologies, functions, behaviors, and life histories (see chapter 16).  

1996 Piraino et al. demonstrated that Turritopsis nutricula, under sublethal stress in laboratory conditions, within 48-72 hours, undergoes ontogenetic reversal at any stage, including the sexual reproduction stage.

The onset of sexual reproduction in this species represents not a point of no return for entering the process of “reverse ontogeny”. Several stressors, which lead to “sublethal stress”, are known to induce “reverse ontogeny”. Among the environmental stressors known to trigger that developmental reversion are starvation, mechanical stress, temperature changes, water salinity, exposure to caesium (an inducer of metamorphosis in this species), and even an intrinsic physiological stressor such as senescence (starting with the sexual maturation of gonads) (Piraino et al. 2004).

Recently, reverse ontogeny is reported in the hydrozoan Laodicea undulata, where the medusa can reverse to a polyp that is capable of reactivating its conventional developmental programme (figure 10.4).

 

 

Figure 10.4. Pathways of transformation from medusa into polyp. Fate of stressed medusae up to 12-tentacle stage (left side), and alternative transformations of stressed or spawning medusae from a 14-tentacle or 16-tentacle stage (right side). The final product is always a polyp colony (bottom), directly or through a resting stage (From Piraino et al., 1996).