PARALLELISMS IN DEVELOPMENT AND EVOLUTION
GIACOMANTONIO
Parallelisms in Development and Evolution
Mike Giacomantonio
Presented to Dr. Bishop
201103983
March 24, 2015
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Since Charles Darwin published The Origin of Species in 1856, biologists have been
conducting research into the evolutionary patterns of organisms. Natural selection, first
described by Darwin, is the gradual process of evolution, by which organisms that are
better adapted for their environment survive longer and pass down heritable biological
traits to their succeeding generations (Elmer & Meyer, 2011, p.296). When evolutionary
patterns disrupt the founding methodology of evolution, research must be conducted to
explain these findings. Often, the answer can be explained through homoplasious
development. This paper will discuss the concept of homoplasy; specifically, the
importance of parallelisms in developmental biology. Furthermore, it will use three
examples to illustrate how parallelisms fit into the theory of homology, and how to use
homoplasy in practical terms. Finally, this paper will illuminate how research into
parallelisms greatly impacts our understanding of constraints on development and
evolution through inherited phylogenetically constrained genes.
The term “homology” is used among biologists to describe characteristics of taxa.
Early definitions, such as by Mayr, state that, “A feature [such as character, structure] is
homologous in two or more taxa if it can be traced back to the same feature in the
presumptive common ancestor of these taxa.” (Mayr, 1982, p.232, cited from Roth, 1983,
p.15). Many criteria are used to determine whether an organism is homologous, including
similarities in developmental origin, structure and anatomical position (Roth, 1983, p.16).
Problems arise when criteria are followed to closely, as many similarities are not of
homologous origin. A popular example of this is the development of octopus and vertebrae
eyes. They are similar in function and construction, however not genetically homologous in
nature (Roth, 1983, p.16). Generally, phenotypes and taxa are believed to diverge over the
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course of evolution, following a homologous path. When confounding variables begin to
question the methodology of the theory of homology however, further explanation is
necessary to rationalize these occurrences (Roth, 1983, p.16).
Homoplasy describes morphological similarities that can be observed in different
organisms, independent of inheritance at the hierarchical level (Wake, Wake, and Specht,
2011, p.1032). Homoplasy can be the result of a reversal to an ancestral trait, or
independent of evolution entirely (Wake, Wake, and Specht, 2011, p.1032-5). Within
Homoplasy are three sub-categories: parallelism, convergence and reversals (Wake, Wake,
and Specht, 2011, p.1032-5). Traditionally these categories were very difficult to
distinguish, however molecular sequence technology can help to reveal differences (Wake,
Wake, and Specht, 2011, p.1032). While parallelisms and convergences are viewed on a
continuum, they are distinct; that is, convergence usually occurs over a greater
phylogenetic distance, and is a result of different genetic mechanisms, whereas
parallelisms typically arise from similar genetic causes (Wake, Wake, and Specht, 2011,
p.1032-5). More specifically, convergences occur as a result of distantly related organisms
having similarities, independent of specific internal constraints (Rui Diogo, 2005, p.736).
Parallelisms on the other hand, are the result of common internal constraints of
homologous genes or developmental pathways, which cause the development of similar
characteristics in multiple but separate lineages (Rui Diogo, 2005, p.736). While the
concept of homoplasy seems straight forward, it has caused problems amongst
phylogenecists, as it can be difficult to apply in a practical context.
Early research on homoplasious development was conducted by Nevo and Beiles
(1988). They performed ecological tests of protein polymorphism in thirteen unrelated
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genera of plants, invertebrates and vertebrates (Nevo & Beiles, 1988, p.229). Their goal
was to determine if natural selection was involved in determining the proportion of
polymorphic loci or their multi-locus structures (Nevo & Beiles, 1988, p.229). Their finding
showed to be inconsistent with the neutral mutation theory of molecular evolution, as
genetic parallelisms were found across most loci and taxa tested (Nevo & Beiles, 1988,
p.242). Average gene diversity and heterozygosity were positively and significantly
correlated with rainfall variation, which suggested that natural selection is an important
evolutionary force at a protein level (Nevo & Beiles, 1988, p.242). This research could be
carried further through the use of molecular sequencing, which allows for the integration
of genetics, and signaling and developmental patterns to become measurable. This form of
technology could significantly advance the range and depth of understanding of phenotypic
evolution, perhaps providing insight into the genetic mechanisms of the macroevolutionary process (Wake, Wake, and Specht, 2011: 1032).
Nevo and Beiles (1988) are among many who have shown that homoplasious
evolution is deeply involved in the evolutionary process, and that it can be traced down to a
protein level. As homoplasious evolution continues to be explored, questions begin to arise
regarding whether ‘parallelisms’ and ‘convergence’ are distinct enough to be dichotomous,
and categorized differently. This idea is debated among biologists across the world, which
has lead to conflicting vocabulary use. Arendt and Reznick (2007) argue that the distinction
between the terms ‘convergence’ and ‘parallelism’ are the result of a time when genetic and
developmental pathways were not understood, and evaluating phenotypic similarity could
not be evaluated accurately (p.31). The term ‘Parallelism’ merely suggests that the
association between taxonomic affinity and genetic similarity may be more probable for
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closely related species than it is distant (Arendt & Reznick, 2007, p.31). Moreover, if these
terms cannot be connected with a clear dichotomy, they should not continue to be used, as
they are responsible for the misleading interpretation of results (Arendt & Reznick, 2007,
p.31). It is argued that instead of having two terms, simply adopting ‘convergent evolution’
as the term to describe the independent evolution of phenotypic similarity would eliminate
all confusion of classification (Arendt & Reznick, 2007, p.31).
While researchers continue to defend the distinction between the two terms,
evolutionary developmental research continues to uncover examples of parallelisms within
nature. Research conducted by Ventura et al. (2011), Reznick and Bryga (1996), and Yoon
and Baum (2003) has found independent cases of genetic parallelisms in gorillas and
chimpanzees, the life history of guppies, and rosette/ inflorescence- flowering plants
respectively. Analyzing each of these cases will help to reveal the importance and necessity
of parallelisms when analyzing homoplasious development.
Gorilla Genome Structural Variation
Ventura et al. (2011) conducted a study that investigated the pattern of structural
variation in the gorilla genome. Genome sequencing and capillary-based clone sequencing
were used throughout the experiment, along with cytogenetic characterization to give
accurate experimental validation (Ventura et al., 2011, p.1640). Within the gorilla genome,
inversions, segmental duplication, deletions and retro-transpositions were all observed
and analyzed, resulting in 7665 structural changes within the gorilla lineage (Ventura et al.,
2011, p.1640). The gorilla’s pattern of genome structural variation was then investigated
using fluorescence in situ hybridization (FISH), which provided a cytogenetic framework of
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large-scale rearrangement events (Ventura et al., 2011p.1641). This was then followed by
completely end sequencing nearly 180,000 BAC clones from a gorilla BAC library (Ventura
et al., 2011, p.1641). The results were then mapped to the human reference genome (NCBI
build 35) to give a clone-based framework of the gorilla genome (Ventura et al., 2011,
p.1641). Finally, blood DNA was obtained from a male silverback gorilla, generating nearly
10-fold effective sequence coverage, using parallel illumine sequencing (Ventura et al.,
2011, p.1641).
The results of their experiment show that the genomes of the gorilla and
chimpanzee have experienced multiple genomic rearrangements that did not occur during
the evolution of the human or orangutan (Ventura et al., 2011, p.1646). Continuous attack
of retroviral integrations on the African ape genome, specifically chimpanzees and gorillas,
has resulted in germline integration after the two lineages diverge (Ventura et al., 2011,
p.1646). Fine mapping of integration sites show that non-orthologous gene displacement is
responsible for genomic variation in the chimpanzee and Gorilla, suggesting ancient
parallelism (Ventura et al., 2011, p.1646). Molecular analysis suggests that this led the two
lineages to both independently acquire subtelometric heterochromatin caps in parallel
(Ventura et al., 2011, p.1646). Thus, the chimpanzee and gorilla genomes are structurally
more derived from the respective properties above, while the orangutan and human
genomes represent the hominid archetype (Ventura et al., 2011, p.1646).
Life-History Evolution in Guppies
Reznick and Bryga (1995) use the life history genotypes of guppies to illustrate the
effect of predation on the genotype. The experiment included a comparison between guppy
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populations in Yarra and Madamas River. Within the two rivers are sites of high and low
predation levels. Comparing and contrasting the life-history patterns of independent
populations of guppies located in two high-predation, and two low-predation sites of the
Yarra River, and then comparing the observed results to results from the Madamas River,
reveals that behavioral and phenotypic differences can be credited to genetic variation
(Reznick & Bryga, 1995, p.347). The results of the experiment showed that guppies from
high-predation sites mature earlier, are smaller in size, reproduce more frequently, yield a
larger number of offspring, and invest a higher amount of resources into reproduction
(Reznick & Bryga, 1995, p.348). These results were then compared to previous research
conducted by Reznick et al. (1995), where the genetic differences in life histories observed
were found to be consistent with life-history phenotypes of the previous research (Reznick
& Bryga, 1995, p.356). The similarities in genetic differences suggest that the similarities in
predation pressure can cause parallel evolution in the life-history (Reznick & Bryga, 1995,
p.356).
Trangenetic Study of Parallelism in Plant Morphological Evolution
Yoon and Baum (2003) conducted a study that focused on possible parallel
evolutions of genetic mechanisms in three independent origins of rosette flowering plants
within the mustard family. Their goal was to evaluate the extent to which the same genetic
mechanism was being used between the different lineages of plants (Yoon & Baum, 2003,
p.6524). Phylogenies show that inflorescence flowering is an ancestral trait, but that
multiple lineages had developed a ‘rosette flowering’ modification independently (Yoon &
Baum, 2003, p.6524). The locus LFY was hypothesized to be involved in the modification,
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because of its heavy involvement in regulating the shoot meristem identity and
architecture in several plant species (Yoon & Baum, 2003 p.6524). By cloning LFY
homologs of the rosette-flowering species, and introducing them to mutant inflorescence
flowering plants, findings could then be compared to the results of the transgenic lines with
control lines to see if the gene expression of LFY loci was associated with rosette flowering
(Yoon & Baum, 2003 p.6525).
The results of the experiment suggest that the LFY loci contributes directly to the
evolution of rosette flowering. However, they did not yield the exact same genetic variation
across lineages, and therefore, the changes that occurred cannot be proven to follow
parallelism (Yoon & Baum, 2003, p. 6528). Remarkably however, the LFY loci is involved in
three independent origins of the same phenotype of rosette flowering plant, which is
known to be a descendant of inflorescence flowering plants (Yoon & Baum, 2003, p. 6528).
This indicates that genetic variation was not random like that of convergence, but was
highly structured by the intrinsic organization of developmental patterns (Yoon & Baum,
2003, p. 6528). Yoon and Baum (2003) conclude by suggesting that developmental
constraint, and therefore parallelism, is the most appropriate source of this genetic
variation (p.6528).
As seen in the three examples above, parallelisms in evolution are very much a
reality when discussing and researching evolutionary development. While many
researchers, including Arendt & Reznick (2007), debate the effectiveness of having
‘convergence’ and ‘parallelism’ as separate terms, evidence suggests that their separation is
absolutely necessary in assessing and understanding evolutionary patterns. Ventura et al.
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(2011) conducted research on the gorilla genome, providing insight into genetic variation
between apes and humans. Reznick and Bryga (1995) showed that environmental
pressures, such as predation, can have a lasting effect on a genome, and also that it will
evolve in parallel with other organisms of that species. Finally, Yoon and Baum (2003)
illustrated the importance of genomic loci on expression of phenotype and other traits.
Unlike convergences, where development occurs independent of genetic input, parallel
evolutionary events suggest that there could be considerable genetic constraint, which
would only allow organisms to adapt in a handful of ways.
The function of gene interaction and its importance on pleiotropic effects is largely
unknown, but may prove to be a fundamental aspect of future research (Elmer & Meyer,
2011, p.303). Recent research in the field of evolutionary development focuses on
understanding genomic architectural design, and the cause-effect relationship with
phenotype. This research could provide concrete evidence for the idea that parallel
evolution is more common in closely related species (Elmer & Meyer, 2011, p.303).
Conversely, it could show whether non-parallel genetic mutations that generate parallel
phenotypes create the same evolution in further downstream pathways (Elmer & Meyer,
2011, p.303). The presence of multiple replicative genetic parallelisms across populations
suggests that there might be a limited phenotypic possibility, or genetic constraint, making
the latter situation much less likely (Elmer & Meyer, 2011, p.304). As Yoon and Baum
(2003) illustrated, it is often difficult to isolate the specific gene responsible for the genetic
mutation, making genetic constraint difficult to prove through experimental context (p.
6528). Often, once the variability of nature and evolutionary pressures are considered, a
universal answer is often unattainable in a laboratory setting (Elmer & Meyer, 2011, p.304,
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Yoon & Baum, 2003, p.6528).
While Wake et al. (2011), along with many others consider homoplasy to be the
diametric opposite of homology (p.1032), Lankester (1870) had originally proposed the
concept of homoplasy as a subcategory of homology (cited from Rui Diogo, 2005 p.735. and
Nixon & Carpenter, 2012., p.161). Additionally, Rui Diogo (2005) argues that evolutionary
parallelisms have been underappreciated because of the difficulty in defining properly the
limits between convergence and parallelisms. While much of Lankester’s work has been
reconsidered, it is obvious that many phenotypic structures that are not inherited arise
during evolution, and can only be attributed to the involvement of inherited
phylogenetically constrained genes (Rui Diogo, 2005, p.736, and Nixon & Carpenter, 2012,
p.161). Lankester’s ‘similarities’ are what we now refer to as parallelisms (Rui Diogo, 2005,
p.736).
Gould (2002) argues that the importance of parallelisms should be revisited, as
recent research has shown that they directly relate to genetic constraint. This idea is
assisted by the discovery that major phyla that have been separated for 500 million years
of evolution still share considerable networks of developmental pathways, deeply rooted in
genetic retention, and inheritance of genetic material (cited from Rui Diogo, 2005, p.736).
With a better understanding of parallelisms in nature, the concept of genetic constraint
becomes much more of a reality.
Ultimately, homology is a fundamental concept that allows us to understand the
mechanisms that dictate evolutionary patterns. When conflicting information arises, such
as that organisms follow homoplasious development, further research needs to be
conducted to understand the complex mechanisms responsible for this evolution. It is also
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important to understand that although homology and homoplasy have their differences,
they share important similarities, as species continue to follow the developmental
pathways of their original phyla. While the distinction between parallelisms and
convergences continues to be questioned by many biologists, the importance of
parallelisms as a distinct category of homoplasy cannot be understated. Ventura et al.
(2011), Reznick and Bryga (1996), and Yoon and Baum (2003) have each conducted
significant research that forwards the understanding of evolution. Technological advances
in evolutionary development have made room for more comprehensive research, which
promotes an understanding of parallelisms on a genetic level, rather than merely a
phenotypic scale. Understanding genealogical discontinuity through convergent evolution
is almost, if not equally as important as understanding similarity through parallelisms, as
comprehending the extent of constraint on systems will be discovered by finding the other
mechanisms present. Finally, current research regarding parallelisms supports the theory
that genetic convergence could be a crucial element in understanding evolutionary
pathways. Continuing research of parallelisms in nature will be crucial in uncovering the
fundamental patterns of adaptive evolution.
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