NELSON R. CABEJ :: Epigenetic Principles of Evolution

EVOLUTIONARY CONVERGENCES: THE TREND TOWARD SAMENESS IN METAZOAN EVOLUTION

There can be little doubt that the tendency to vary in the same manner has often been so strong that all the individuals of the same species have been similarly modified without the aid of any form of selection.

C. Darwin

Evolutionary convergences represent a ubiquitous phenomenon in the kingdom Animalia. They represent an adaptive evolutionary trend resulting from systematically acting principles. Empirical evidence lends no support to the neoDarwinian principle that similar evolutionary pressures arising from similar conditions of living of two or more biological taxa lead to their phenotypic convergence. It has never been demonstrated that evolutionary convergences may result from evolution of similar genetic changes in converging species or other taxa. In the course of their evolution metazoans, to an incredible extent, have conserved the function of their genes, GRNs (gene regulatory networks) as well as developmental pathways. The failure of attempts to show that genes may play any role in evolution of phenotypic convergences in metazoans, suggests that the epigenetic view that evolutionary convergences arise from activation of similar/identical developmental pathways deserves serious consideration.

Predictability in Metazoan Evolution:

Evolutionary Sameness

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Evolutionary Convergences

Evolutionary convergences imply the independent development of the same character in two or more lineages not linked by common descent. The concept of the evolutionary convergence does not imply identicalness of convergent structures rather a general visually perceived phenotypic similarity.

Evolutionary convergence seems to be a more widespread phenomenon than is generally realized (Hodin, 2000) and the ubiquity of the phenomenon in the kingdom Animalia makes its study crucial for understanding mechanisms of evolutionary change. From a theoretical standpoint, the ubiquity of evolutionary convergences suggests that evolution of living forms may not be simply a contingent process of exclusively unpredictable outcomes.

Evolutionary convergences are evolutionary innovations. For such innovations to occur, new epigenetic information has to somehow be acquired and invested for producing them. But being not machines of unlimited problem-solving and information generation; metazoans often fail to produce evolutionary innovations and this may dam up evolution in certain directions. Such situations are commonly described as evolutionary constraints. When more than one taxon is stuck in the same evolutionary dead end, biologists speak of evolutionary convergence. This is obligatory convergence. Sometimes, different taxa confronted with similar evolutionary pressures may independently evolve similar developmental pathways as optimal solutions to these pressures, which may be described as convergence by optimization.

Evolutionary Convergences in the Animal Kingdom

For a convenient and updated information on the ubiquitousness of evolutionary convergence and the pervasiveness of convergent evolutionary phenomena in metazoans I would recommend the very informative review by Barlow (2003). Among the most eloquent examples included in that review are: evolution of wings from forelimbs in birds and mammals (bats); evolution of flightlessness in insects and birds after migrating to islands; independent evolution of flightless vegetarian birds in Africa (ostriches), South America (rheas), Australia (emus) and Madagascar (“elephant birds”); repeated independent evolution of gas bladders in fish and female octopuses; of venomous bite in snakes and at least two small Caraibean mammals; evolution of bioluminescence in numerous deep sea fish and insects; echolocation (ultrasonic hearing) in insects, birds (several owl species) and mammals (whales and bats); independent evolution (10 times) of venomous sting in taxa ranging from lower vertebrates, such as coelenterates (jellyfish) to arthropods (mollusks, spiders and insects), vertebrates such as fish, reptilians (snakes) and even mammals (male duckbill platypus); use of magnetically charged particles of magnetite for orientation during migration in butterflies, fish, and birds; evolution of external organs for producing auditory signals and songs in insects and American tropical birds (manakins); evolution of eusociality, i.e. living in colonies, implying division of labor and castes of distinct morphological, behavioral and life history traits, etc.

Convergent Evolution of Eyes

From the neoDarwinian view, evolution of complex structures such as eyes through accumulation of small gradual changes under the action of natural selection could not have happened more than once, and extant species should have inherited it as a homologous organ from their common ancestor. Nevertheless, the eye is an often-quoted example of convergence thought to have independently evolved about forty to seventy times in the course of metazoan evolution (Salvini-Plawen and Mayr, 1977).

We know that the development of eyes in species as different as humans and Drosophila involves, and is under control of, the same basic homologous genes Pax-6, which, despite mutations, which it has been subject to, has amazingly remained functionally unchanged after more than 500 million years of separate evolution of these taxa. During this evolutionary long period of time, the gene has little changed structurally as well: the Drosophila Pax-6 shows high amino acid sequence identity (94%) with Pax-6 of quail, mice, and humans (Quiring et al., 1994). It is noteworthy that with the same basic control gene and with the same highly conserved gene regulatory network organisms belonging to very remotely related taxa such as mammals and cephalopods (octopuses and squids) have evolved similar camera eye structures (figure 18.1).

Figure 18.1. Controller of all eyes? Possible sites of action of Pax-6 in the development of three very different types of eyes – human (vertebrate), octopus (cephalopod), and the compound eye of Drosophila (From Zucker, 1994).

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Convergence of Electrical Organs and Electroreception in Fish

Striking examples of convergence are observed in electric fish of distantly related groups, such as Mormyriformes of Africa and Gymnotiformes of South America, which share no common electrogenic or electrosensory ancestor (figure 18.2). Special structures and physiological mechanisms for emitting and receiving electrical signals have independently evolved several times in these two groups. Both groups have also independently evolved sinusoidal wave-type electrical organ discharges (EOD) of constant rates and pulse-type, separated by long intervals; furthermore, both groups have evolved three types of electroreceptors with distinct functions While insects and other invertebrates have five times independently evolved compound eyes, with numerous ommatidia as the basic unit of visual reception, the camera eye evolved independently at least seven times in both vertebrates and invertebrates and separate pathways of transmission of electrical signals.

Differences in the neural basis of differential phase comparisons are identified even within the group of mormyrids [in Gymnarchus Differences in the neural basis of differential phase comparisons are identified even within the group of mormyrids [in Gymnarchus comparisons are made in the hindbrain, whereas in Brienomyrus - in the midbrain (figure 18.3)], and Gymnarchus commissural pathway for time coding is not found in other African mormyrids], there is a striking similarity in the rhythm control mechanisms in the pacemaker as well as in computational algorithm for the jamming avoidance response between the African mormyrid Gymnarchus and the South-American Eigenmannia.

Evolutionary Convergences of the Nervous System

These convergences is believed to have arisen from similar intrinsic pressures for computational capabilities (Nishikawa, 2002; Carr and Soares, 2002; Eisthen and Nishikawa, 2002). Striking similarities are observed among brainstem circuits encoding auditory signals in birds and mammals (Carr and Soares, 2002). As for the widespread convergences in the structure and physiology of the central nervous systems, it is thought that they result from the properties of neural circuits rather than any changes in genes (changes in properties of neural circuits are related to changes in organization of neural circuits, which involve no changes in genes).

Figure 18.2. Cladogram illustrating convergent evolution of wave-type electric organ discharge (EOD) and jamming avoidance responses in African mormyrid and South American gymnotid fish. The common ancestor of mormyrids and gymnotids was non-electrogenic. Wave-type EODs and jamming avoidance responses evolved independently in Gymnarchus and in the common ancestor of Eigenmannia and Apteronotus. Sternopygus possesses a wave-type EOD but lacks a jamming avoidance response (From Nishikawa, 2002). Finally, and more surprisingly, both distant groups have independently evolved similar neural networks in the brain for changing their own EOD frequencies in cases of jamming from conspecific EODs (Nishikawa, 2002).

Figure 18.3. Time-coding pathways in the gymnotiform Eigenmannia compared with those in the mormyrids, Brienomyrus and Gymnarchus. (a) In Eigenmannia, the time-coding electroreceptor (T receptor) projects to spherical cells in the ELL. The spherical cells send axons to the midbrain torus layer VI where they terminate on the distal dendrites of small cells, and on the somata of giant cells. Giant cells send large axons to distant small cell targets. Small cells presumably act as coincident detectors, and fire only when the phase of the stimulus in body region A (phase A), differs from the phase of the stimulus in body region B (phase B), by a precise time difference. (b) The Brienomyrus time-coding pathway begins in the periphery with the Knollenorgan receptor, and leads to the spherical cells in the nucleus of the ELL (nELL) in the hindbrain. These giant cells project bilaterally to the ELa of the midbrain where they terminate on large and small cells with electrotonic synapses. The large cells, which are GABA-ergic, terminate on small cells within the nucleus. Rather than being coincidence detectors, the small cells appear to be selectively blanked, depending on the delay of the inhibitory input from the large cells. (c) The Gymnarchus time-coding pathway resembles the Knollenorgan pathway only remotely. The S-receptor, which is phase-locked to the EOD stimulus, sends large axons to terminate on giant cells in the ELL, but collaterals also terminate in the ICL of the ELL where differential phase-sensitive cells are found. Giant cells also send axons to converge on the same cell layer, and although the circuit is unknown, the cells in the ICL appear to be acting as coincident detectors. Temporal analysis is accomplished entirely in the hindbrain in Gymnarchus.

Abbreviations: ELL, electrosensory lateral line lobe; ICL, inner cellular layer of the ELL medial zone; nELL, nucleus of the ELL; ELa, nucleus exterolateralis pars anterior (From Hopkins, 1995).