Stanford University Reasons for Absence of Organism Discussion Many types of organisms did not, do not, or never could exist. Speculating about the reason
Stanford University Reasons for Absence of Organism Discussion Many types of organisms did not, do not, or never could exist. Speculating about
the reasons for such absences can be quite useful. In the essay, briefly
summarize the authors’ hypothesis. Then indicate what observations or
experiments could be done to verify or cast doubt on the explanation.
Before choosing a topic, please read Vermeij, 2015 (attached) on forbidden
phenotypes.
Alternatively, you can propose your own hypothesis, together with an appropriate
test.
two pages double spaced
Here are some examples of organisms that are either unknown or very rare in
nature, either today or in the past:
Phantom organisms: animals moving with wheels. See M. La Barbera,
1983, Why the wheels won’t go. American Naturalist 121: 395-408.
Aerial phytoplankton (organisms photosynthesizing while floating in the air):
phytoplankton are very common in water, and such tiny organisms as
bacteria, spores of plants, and insects are common in the aerial plankton.
So why not photosynthesizing aerial phytoplankton?
Freshwater hermit crabs: hermit crabs live in the empty shells of snails. The
shells become empty upon the death of the snails that built them. Hermit
crabs are common in the sea and, in the tropics, also live in coastal zones
of the land. Why not in fresh water? See Vermeij, G. J., 1987, Evolution
and Escalation: An Ecological History of Life, Princeton University Press,
Princeton (especially Chapter 8).
Marine insects. There are millions of species on land, but only about 1400
in the sea, and most of those live on the seashore. See G. J. Vermeij and
R. Dudley, 2000, Why are there so few evolutionary transitions between
aquatic and terrestrial ecosystems? Biological Journal of the Linnean
Society 70: 541-554.
Strong fliers that eat leaves: Very few actively flying birds and mammals,
and even insects, have a diet consisting mainly of green plant leaves. See
R. Dudley and G. J. Vermeij, 1992, Do the power requirements of flapping
flight constrain folivory in flying animals? Functional Ecology 6: 101-104.
No small marine mammals: there are small marine birds, so why no marine
mammals smaller than sea otters?
Photosynthesizing mammals or birds: Many marine animals, mostly
sedentary forms like clams and corals, can filter-feed and photosynthesize
at the same time. So why don’t fish, birds, mammals, or insects do it?
Live-bearing birds. All birds lay eggs, most mammals bear live young. Why?
See R. M. R. Barclay, 1994, Constraints on reproduction by flying
vertebrates: energy and calcium. American Naturalist 144: 1021-1031.
Vines climbing to the forest canopy in cold-temperate forests. Such vines
are very common in the tropics and in warm-temperate woods, but rare in
conifer-dominated cold forests. See Vermeij, 1987, Evolution and
Escalation, An Ecological History of Life, Princeton University Press,
Princeton (Chapter 2).
Modern land animals the size of dinosaurs: large size was all the rage
among dinosaurs of the Mesozoic, but no mammal came anywhere close
to their size. Neither have modern crocodiles or other reptiles. Why not? Downloaded from http://rsfs.royalsocietypublishing.org/ on November 9, 2015
Forbidden phenotypes and the limits
of evolution
rsfs.royalsocietypublishing.org
Geerat J. Vermeij
Department of Earth and Planetary Sciences, University of California, Davis, CA, USA
Review
Cite this article: Vermeij GJ. 2015 Forbidden
phenotypes and the limits of evolution.
Interface Focus 5: 20150028.
http://dx.doi.org/10.1098/rsfs.2015.0028
One contribution of 12 to a theme issue
‘Are there limits to evolution?’
Subject Areas:
biochemistry
Keywords:
evolution, phenotypes, limits, metabolism,
natural selection
Author for correspondence:
Geerat J. Vermeij
e-mail: gjvermeij@ucdavis.edu
Evolution has produced an astonishing array of organisms, but does it have
limits and, if so, how are these overcome and how have they changed over
the course of time? Here, I review models for describing and explaining
existing diversity, and then explore parts of the evolutionary tree that
remain empty. In an analysis of 32 forbidden states among eukaryotes,
identified in major clades and in the three great habitat realms of water,
land and air, I argue that no phenotypic constraint is absolute, that most
constraints reflect a limited time –energy budget available to individual
organisms, that natural selection is ultimately responsible for both imposing
and overcoming constraints, including those normally ascribed to developmental patterns of construction and phylogenetic conservatism, and that
increases in adaptive versatility in major clades together with accompanying
new ecological opportunities have eliminated many constraints. Phenotypes
that were inaccessible during the Early Palaeozoic era have evolved during
later periods while very few adaptive states have disappeared. The filling of
phenotypic space has proceeded cumulatively in three overlapping phases
characterized by diversification at the biochemical, morphological and
cultural levels.
1. Introduction
Making sense of the vast diversity of life is one of the great intellectual challenges of evolutionary biology. Over the course of its history, life has
blossomed into a seemingly endless array of phenotypes (shapes, habits and
physiologies), and the evolutionary tree is made up of countless branches
(clades) and twigs (lineages), some prematurely pruned by extinction, others
sprouting new shoots. Despite this variety, there is empty space in the tree,
implying the existence of limits to evolution. It is this empty phenotypic
space with which this paper is concerned.
2. Approaches to diversity
Two complementary approaches have dominated the description of and explanation for diversity. These are (i) the biodiversity approach, which documents
the characteristics, origins, extinction, distribution and phylogeny of taxa,
lineages and clades in space and over time and (ii) the structural approach,
which uncovers the mechanics by which genes and their interactions orchestrate
growth, development and evolutionary innovation.
A third perspective on diversity interprets it as an inevitable consequence of
random variation that accumulates in a system of initially similar parts whose
numbers multiply. This view, dubbed the spreading principle [1] of the zeroforce evolutionary law (ZFEL) [2], holds that diversity arises even in the absence
of constraints or forces acting on the parts. The ZFEL represents the null model
against which patterns imposed by structural protocols, material constraints or
natural selection must be compared. In Raup & Gould’s [1] slightly different
version, each variation may be adaptive, but the aggregate pattern can be
described (if not explained) by random walks. In the special case of size evolution [3,4], the small-bodied ancestor in a major animal clade tends to give
rise to larger descendants simply because evolution towards smaller size is
& 2015 The Author(s) Published by the Royal Society. All rights reserved.
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Any phenotypic change must be compatible with a living
body that performs adequately at all stages of the life cycle.
The pattern and materials of construction and modifications
to them must conform to functional demands throughout
life, from the zygote to the adult. Besides limits imposed by
physics and chemistry, impediments to phenotypic evolution
are often attributed to developmental constraints [5], but in
reality they are due to natural selection, which distinguishes
between what works and what does not work given the
organism’s circumstances.
Akin to a developmental constraint is the phylogenetic
constraint, a historically preserved, invariant property possessed by all members of a clade. Any phenotypic variation
that does occur within the clade is channelled in only a few
directions [6]. To be sure, all lineages are marked by the
stamp of history: an ancestor possesses particular, contingent
traits that evolved under specific, contingent circumstances,
and these traits are passed on to descendants [7]. However,
this ancestral influence wanes as conditions change, new
opportunities emerge and constructional innovations arise
[8]. Phylogenetic constraints must therefore be universal in
the short run, because no lineage lives everywhere or can
do everything; but invoking such constraints in general
does little more than restate the problem of limitation rather
than offer an explanation for structures unrealized and
adaptive pathways not taken.
The constraints imposed by ancestors and by the evolved
body-plan construction of major clades are enforced by natural
selection and therefore by the circumstances in which organisms develop and evolve. But natural selection also plays a
role in lifting constraints, as discussed in the next section.
4. Versatility
Potential phenotypic diversity depends on the number of parts
of the body (modules, domains or compartments) that are
individuated [9]. These parts are semi-autonomous units that
function and are constructed separately from other parts
with which they share a common developmental origin and
fate. The envelope of design possibilities is small when there
are just a few modules, because any change will affect the
function and performance of much or all of the developing
body. As the number of modules increases, interactions
and signals among parts become more localized, functions
become more autonomous, and performance trade-offs
among functions and among parts recede. The result is greater
adaptive versatility [8,10], which enable a given body plan
of construction to generate a greater variety and range of
5. The time– energy budget constraint
The alleviation of functional trade-offs associated with an
increased versatility arises from an expansion of an individual’s time–energy budget. This is expressed as an increase in
metabolic rate and metabolic scope (the difference between
resting and active work by an organism). Individuals with
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3. Selection and constraint
adaptive phenotypes. Wagner [9] presents a comprehensive
account of the mechanisms involved.
Within major animal and plant clades, younger branches
are morphologically more versatile than older ones. Shell
geometry in gastropods indicates a single module in the
early-diverging Patellogastropoda and Vetigastropoda, and
two or three modules in the later-appearing Caenogastropoda and Heterobranchia [11 –13]. The segments and limbs
of early arthropods show less functional differentiation than
more derived clades [14–16]. When intercalary growth
evolved in plant leaves, a greater variety of leaf shapes and
venation patterns became possible [17,18]. Other examples
come from jaw and skull evolution in fishes [19 –23] and
the plastron of atelestomatan (‘irregular’) sea urchins [24].
This widespread trend is consistent with the ZFEL but is
not explained by it. The new dimensions in which variation
is expressed are controlled by genes and their interactions;
and the modules that are free to vary are subject to relentless
selection as they interact with each other within the ecosystem
of the developing body [25]. At the very least, therefore, the
diversification of parts of a system in the absence of external
constraint is strongly enhanced by regulation and limits
enforced by selection.
A more compelling case for a large role for the ZFEL can
be made for unregulated exploration of design space early in
the history of major clades. This kind of variation has been
documented in Early Cambrian lapworthellids [26], segment
number in early trilobites [27– 29], plate numbers and positions in early pelmatozoan echinoderms [30–32] and the
pattern of tertiary and higher order veins in the leaves of
early angiosperms [33].
Gould [34] suggested that organisms reproducing when
in an ontogenetically juvenile stage are able to add major
innovations and to change adaptive direction more readily
than can those in which reproduction takes place at a later
developmental stage. He argued that regulation of development has broken down in these progenetic lineages, not
least because the time interval over which the body is
tested is short. Gould [34] noted that early members of
most major animal clades were small and that many of the
specializations attending large size were dispensable [3].
Innovations associated with miniaturization and truncated
development have been identified in the origins of angiosperms with high leaf-vein density [18] and in the origin of
birds [35].
In short, the regulated plasticity and increased versatility
and replaced unregulated variation are outcomes of natural
selection. Versatility opens up new phenotypic territory for
selection and adaptation by expanding the dimensionality
of ontogeny and by making accessible new directions of
diversity and specialization. In the next section, I argue that
a larger time– energy budget, favoured by competitionrelated selection, is the crucial factor linking versatility,
selection and the lifting of constraints.
rsfs.royalsocietypublishing.org
less likely. The resulting pattern, in which the mean or
median size within the clade increases over time, looks like
directional evolution but is instead adequately described as
random variation. Causal explanations are, however, still
needed for the evolution of size in particular lineages.
These three approaches explore the diversity that exists.
Complementing these perspectives is a fourth, motivated
by the question whether and which phenotypes have failed
to evolve. Here, I employ this approach to investigate
empty parts of the evolutionary tree and the constraints
that are responsible for these voids.
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How do these ideas about constraint apply to phenotypes
that do not exist? To answer this question, we must call on
our imaginations and knowledge of existing diversity to
conjure up organisms that make functional sense but that
have never evolved or have done so only under very limited
circumstances. This is not a frivolous exercise; on the contrary, it forces us to test the limits of our understanding of
development, selection and history. The 32 phenotypes I discuss in the following sections (summarized in table 1) often
point to energetic limitations, but they also lay bare empty
space in our evolutionary understanding.
The cases discussed below are not exhaustive. For example,
I do not discuss size limits, which are imposed by a combination of material constraints, the physical environment and
the size-dependent acquisition, retention and internal transport of nutrients, gases and metabolic products. Despite
6.1. Wheels
No animal uses wheels to move about, presumably because
suitable expanses of pathways of flat, even ground are for the
most part unavailable in nature [39] and perhaps also because
structures like wheels that rotate without limit and in a consistent direction on an axle are difficult to build in the context of a
developing animal body. Some whole organisms form almost
perfect spheres or wheels by rolling up so that the front and
hind ends touch, enabling the animal to roll away from
enemies [40]. Examples include some terrestrial caterpillars,
cockroaches, isopods, millipedes and spiders, and marine
stomatopod larvae and fossil trilobites [36,41]. Active rolling
is achieved in some spiders [40] and in scarabaeid dung bettles.
The latter roll dung balls and may even climb onto and ride
these balls to prevent overheating [42,43]. Rotation is known
in flagella and, in modified form, in the screw-like leg joints
of curculionid weevils [44], but none of these cases amounts
to wheeled transport.
6.2. Pollination and dispersal
Plants with aerially emergent flowers are often assisted in sexual
reproduction by mobile pollinating animals, which often fly fast
and over long distances between flowers. With the possible
exception of short-distance pollination of seagrasses by fishes
[45], there is no evidence that water-dwelling organisms are
aided in cross-fertilization by aquatic animal vectors. The effectiveness of gamete dispersal in the buoyant medium of water
may erase any benefit that animal assistance can offer. Moreover, small animals are more constrained in the speed and
distance of movement in water than in air [46]. The same explanation may account for the rarity of animal-mediated dispersal
of propagules in aquatic (especially marine) habitats. Animalassisted dispersal of spores, seeds, fruits and small organisms
is extremely widespread on land. Some intertidal marine gastropods and many small freshwater animals are dispersed by birds,
but evidence of dispersal of water-dwelling algae and animals
by mobile aquatic animal vectors is limited. Algal fragments
and small animals can be locally dispersed after surviving
passage through the digestive systems of animals [47]; and
freshwater unionioidean bivalve larvae parasitize and are
dispersed by fishes. Parasitic species without a free-living
stage also depend on their hosts for dispersal, but the primary
host is often a bird or other land-derived animal. Marine
animal-assisted dispersal before the evolution of marine tetrapods may therefore have been even less common than it is today.
6.3. Biomineralization
Biomineralization, the formation of calcium- and silicon-based
minerals inside or outside the body, is extremely widespread
in multicellular organisms and has evolved dozens of times
[48–53]. Nevertheless, there are major clades in the tree of
life in which biomineralization has apparently never evolved
(table 1). In some cases such as insects and several other
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6. A catalogue of forbidden phenotypes
general scaling laws, size limits are rarely absolute and have
been frequently transcended over time in major clades. I also
mostly exclude limits imposed by structural materials (but
see the section on biomineralization below). Animals often
rely on materials they do not themselves synthesize, implying
that material constraint can be overcome by exploiting already
existing sources.
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faster metabolism gain a competitive advantage, but also
require access to a high, predictable supply of resources; and
those resources are largely controlled by the ecosystem—the
totality of organisms and their interdependencies—in which
individuals are embedded. Three pathways are available for
raising the time–energy budget: (1) increasing the density
and effectiveness of energy-acquiring or energy-producing
structures, (2) entering into a stable, intimate partnership or
trading relationship with organisms that possess complementary capacities, and (3) living in a warm environment
where all processes are faster and where many functions are
energetically less costly.
Besides relieving trade-offs, greater versatility and the
expanded time–energy budget offer many competitive benefits.
These include rapid growth, high fecundity, greater investment
in offspring, the production of energy-rich defensive compounds, forceful aggression and feeding mechanisms, internal
physiological homeostasis (a well-regulated internal state),
sophisticated coordination between sensory and motor networks, rapid immunological responses, fast and sustained
locomotion, and elaborate displays associated with mate
choice. With a larger time–energy budget, passive feeding
and defence and conformity of internal conditions to the external environment give way to more active responses and to
greater internal control [36,37]. Versatility may arise under permissive conditions, but its potential is realized as competition
propels lineages to occupy many roles in ecosystems.
Of course, constraints remain; but selection under an
increasing range of circumstances—most of them created or
modified by life itself—has globally pushed back the limitations under which multicellular living things evolve and
operate. The extent to which selection does so depends on
the supply and accessibility of resources. Animals in much
of the deep sea are severely constrained by cold and a
meagre nutrient supply. Freshwater habitats can be productive, but most are island-like. We have shown that the
intensity of competition and predation on remote terrestrial
islands (and by extension in freshwater) is less than in similar
mainland or oceanic habitats [38]. Large productive ecosystems in which the community as a whole regulates and
stabilizes consumption, production and resources permit
the highest diversity of phenotypes and ways of life without
completely eliminating evolutionary constraints.
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Table 1. List of forbidden phenotypes among living multicellular organisms.
4
biomineralization in fungi, Ctenophora, Platyhelminthes, Nematoda, Chelicerata, Myriapoda, Hexapoda, Hemichordata and Bryophyta
rigid reef-like structures in freshwater
bioerosion in freshwater
conchicoly (living in and moving about in shells after the death of the original builder) in freshwater
endothermy in Ctenophora, Cnidaria, Porifera, Platyhelminthes, Nematoda, Crustacea, Chelicerata, Myriapoda, Lophotrochozoa, Hemichordata, Tunicata,
non-methanogenic Archaea in parasitic or mutualistic partnerships with eukaryotes
photosymbiosis in Ctenophora, Bryozoa, Cirripedia, Echinodermata, fishes and flying animals
chemosymbiosis in Cnidaria, colonial animals, Porifera, Cephalopoda, Echinodermata, Tunicata, Chordata, terrestrial animals and planktonic animals
aerial phytoplankton
capture of living animals by plants and algae other than angiosperms
specialized scavenging in mammals
annual herbaceous growth in land plants outside angiosperms
woody stems in bryophytes
basal leaf (or blade) growth in plants and algae outside angiosperms and laminarialean algae
roots for sedimentary uptake of nutrients in algae outside siphonalean and charophyte green algae
herbivory in Ctenophora, Porifera, Cnidaria, Platyhelminthes, Araneae, Myriapoda, Scaphopoda, Cephalopoda, Chondrichthyes, adult Amphibia and Serpentes
algal diet in marine turtles and marine birds
piercing-and-sucking herbivory on freshwater vascular plants by insects
gelatinous freshwater plankton
envenomation in Porifera, Ctenophora, Crustacea, Hemichordata, Tunicata, Bryozoa, Brachiopoda, water-dwelling plants, algae and fungi
gastropod opercula that bite
communication by sound in basal Metazoa, Lophotrochozoa and Echinodermata
communication by electrical signals in basal Metazoa, Ecdysozoa, Lophotrochozoa and Echinodermata
social organization in shell-bearing Mollusca, Echinodermata
eusociality in Lophotrochozoa, Echinodermata and Chordata outside Mammalia
combinatorial communication among animals other than humans
clonal reproduction in Mollusca, Brachiopoda, vertebrates and Arthropoda
live-bearing in turtles and birds
arthropod groups, the skeletal function of mineral…
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