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Many fruits are not homologous, originating from different parts of a plant. Yet they all have similar properties:
Ripe fruits all have yellow to dark red color
They all have a lot of water and sugars, even in dry climate where water is in shortage.
Besides sugars they usually have acids making them sour to sweet in taste
I understand that these possibly developed as a contract between the plants and the animals in that the plant would provide beneficial fruit tissue so that the animal to swallow the seed so to propagate it for longer distances.
But I wonder, why there are no fruits that would imitate the taste of meat, nuts, seeds, foliage, grass, mushrooms, roots, milk and other food sources, common for the animals?
Why there are no salty fruits for instance or those rich in proteins rather than sugar and water, or having the smell of carrion?
Howe and Smallwood (1982) provide a nice review of the many methods of seed dispersal that have evolved in plants. The review is broad but they do have a section on frugivory. They highlight hypotheses developed by McKey, and Howe and Estabrook (see Howe and Smallwood for citations) that suggest plants may use one of two strategies.
One strategy is the "high investment model." Plants invest lots of resources to produce large seeds and nutrient rich fruits. THe hypothesis is that these types of fruits tend to attract relatively few but specialized frugivores that are will to invest the energy necessary to find these types of fruits and their associated nutritional reward.
The second strategy is called the "low investment model." In this model, plants invest little in individuals seeds and fruits but produce an abundance of them. The hypothesis is that these types of fruits will be eaten by as many different potential seed dispersers as possible. These tend to be very small or starchy although they can still be colored as you describe.
Other factors also come into play. For example, tropical fruits tend to have large seeds and nutrient rich pulp while temperate fruits tend to be smaller and offer less nutritional reward. All of this is placed in the context of the community diversity of frugivores. The Howe and Smallwood paper was an interesting read.
A paper by Gatier-Hion et al. (1985) looked at the characters of fruit choice and seed dispersal mechanisms by tropical forest vertebrates. The showed the relationships between fruit characteristics and the corresponding frugivores. They looked at 122 different fruit species and the frugivores that consumed them. Their results showed that fruits tended to separate along one of three axes:
- Heavy, indehiscent fruits with fibrous flesh and well protected seeds vs light, dehiscent fruits with unprotected seeds. Many of small fruits are red,
- Lots of seeds produced (typically the the large indehiscent) vs few seeds produced, and
- Juicy and brightly colored fruits vs dry and dull-colored fruits.
Figure 2 from Gautier-Hion et al., shown here, shows the relationship between different frugivores and the fruit types. Notice that small granivores, which are frugivores, don't eat large, juicy fruits. They consume lots of small green or brown grains that are easy to manipulate and produced in high quantities. Squirrels are similar.
Thus, as you suspected, fruits and seeds have evolved in response to their frugivores but the fruits do not always have the traits you listed. I think, but do not know for certain, that the fruit traits you list are the result of selection being driving by the frugivores. The sugars provide lots of quick energy, which is necessary for active animals. The carbs probably provide a much greater nutritional reward than salts or proteins (which are present anyway). The colors may help the fruits to stand out against the green foliage (for organisms that are not red-green colorblind). These traits probably provide the greatest reward (lots of energy) with the lowest energy investment by the frugivore (easy to find).
Throughout, I've assumed natural conditions and not fruits modified by artificial selection for human consumption.
Gautier-Hion, A., et al. 1985. Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia 65: 324-337.
Howe, H.F. and J. Smallwood. 1982. Ecology of seed dispersal. Annual Reviews in Ecology and Systematics 13: 201-228.
How are you defining fruits? Because if you count any seed body of a flowering plant, you must include several items commonly described as vegetables, including pumpkins, zucchini, squash, cucumber, peppers, etc. And there are other colors of fruit, such as blue berries. These all serve similar functions for the plant, something eats the fruit, then deposits the seeds somewhere else.
If you define a fruit by what the average person calls fruit, then you've biased the population because humans have selected for juicy sweet tasting fruits over thousands of years of breeding. Humans like large sweet tasting fruits, so they selected for those traits, driving most fruits to have those traits. Wild fruits probably have much more diversity, and there would much less distinction between fruit and vegetable.
Many of us were inspired, at an early age, by Hedberg  and Carlquist  describing the bizarre, unbranched shrubs with massive leaf rosettes that dominate equatorial alpine zones in many parts of the world. Such plants share a highly unusual climate - 'summer every day, winter every night'  - and a highly unusual growth form characterized by large woody stems, extensive water-storage tissue in the stem pith and large leaves that persist on the stem after they die and, while alive, often curl around the terminal bud at night or impound rainwater surrounding that bud. These traits appear to be adaptations to nightly frosts, insulating vulnerable buds and water-storage tissue from a few hours of low temperatures, facilitating relatively rapid growth away from the ground where the highest diurnal fluctuations in temperature occur and providing moisture to permit photosynthesis during morning droughts when the sun is up but the ground still frozen [3–5]. These rosette shrubs - belonging to the families Asteraceae, Lobeliaceae, Valerianaceae and Bromeliaceae - appear to be striking manifestations of convergent evolution, of the independent acquisition of similar adaptations to similar environments by members of distantly related lineages.
This story became even more remarkable when it was later confirmed, by phylogenetic analyses of DNA sequences [6–8], that rosette shrubs had evolved independently at least three times in Asteraceae alone, including Dendosenecio of tribe Senecioneae on the volcanoes of tropical East Africa, Espeletia of tribe Heliantheae subtribe Melampodiinae in the northern Andes, and the silverswords (Arygyroxiphium) of tribe Heliantheae subtribe Madiinae of the Hawaiian Islands. DNA sequences - especially of non-coding regions with little or no possible selective value - have an advantage for analysing phylogenetic relationships among species invading extreme environments and/or undergoing adaptive radiation on islands or island-like habitats. In such situations, morphology is likely to often be a poor guide to ancestral relationships, given the strong selection on members of different (but perhaps closely related) lineages to converge in form and physiology in an extreme habitat, and on members of a given lineage to diverge from each other after invading a new area .
Like Asteraceae, Lobeliaceae (about 1200 species) is composed primarily of herbaceous plants from temperate and subtropical areas. However, in Lobelia and several closely related genera, woodiness has evolved in > 450 species, and 'giant' pachycaulous rosette shrubs grow in alpine areas and subalpine bogs of East Africa, South Asia, Polynesia, Hawaii and the Brazilian Shield and in semi-arid areas of Chile unbranched or sparsely branched species with somewhat more slender stems occur in montane forests in these areas and the Andes. Hedberg and Carlquist suggested that giant woody lobeliads from high elevations in East Africa and Hawaii were convergent on Afroalpine Dendrosenecio, Andean Espeletia, and Hawaiian Argyroxiphium. Carlquist [10, 11] argued that these giant rosettes and related woody species in both areas evolved ultimately from herbaceous ancestors, while Mabberley [12, 13] instead argued that the pachycaul habit was primitive, with giant rosette shrubs and allied woody species with more slender stems forming a single worldwide lineage, with high-elevation species being derived from less specialized forms at mid elevations and with herbaceous Lobelia being derived independently from different woody sublineages. To complicate matters further, several botanists had proposed that the endemic Hawaiian lobeliads were not all closely related to each other but, instead, represented the product of up to five long-distance dispersal events (see review by Givnish et al. ).
Over the past 16 years, several groups have attempted to use molecular data to analyse relationships and patterns of adaptive evolution and geographic diversification among giant woody lobeliads and allied species. Knox et al.  used plastid DNA restriction-site data to show that woody tetraploid species of Lobelia and related genera from East Africa, Hawaii, Polynesia, the Bonin Islands, South Asia and Chile formed a clade and that they were derived from herbaceous ancestors. Knox and Palmer  used plastid DNA sequences to show that the giant and woody species of Lobelia from East Africa formed a clade, with the exception of a few Brazilian species derived via trans-Atlantic dispersal. Their phylogeny implied that the most specialized, giant-rosette shrubs of the Afroalpine zone (for example, Lobeliaceae deckenii, L. rhynchopetalum, L. telekii, L. wollastonii) evolved from ancestral, unbranched mid-elevation species with more slender stems, similar to present-day L. giberroa - supporting one of Mabberley's proposals. Givnish et al.  used plastid sequence data to show that the Hawaiian woody lobeliads are monophyletic that they colonized the Hawaiian archipelago 13.0 to 13.6 million years ago, based on independent calibrations based on the ages of islands to which present-day species are restricted or the ages of fossil Asterales that the giant species of Lobelia sect. Galeatella of subalpine bogs and grasslands are apparently derived from mid-elevation ancestors with more slender stems, similar to those of present-day Clermontia, Cyanea and Delissea and that their closest relatives are the woody lobeliads of East Africa, Polynesia/Bonin Islands and South Asia.
Antonelli  has now addressed several of these same questions - and, most notably, the question of whether giant woody lobeliads are the product of convergent evolution or are instead all closely related - in a new phylogenetic study based on the most comprehensive set of lobeliads sequenced to date (101 spp.). This investigation has much to recommend it. First, it documents an 'Out of Africa' scenario for the origin of Lobeliaceae, based on the large number of small annual herbs native to Africa that form a grade just above the basal node of the family. Second, it confirms the hypothesis advanced by Knox et al.  that woody lobeliads evolved from herbaceous ancestors. Third, it confirms and extends findings by Knox, Givnish and their colleagues that lobeliads have repeatedly dispersed across the Atlantic and Pacific Oceans, with the new data supporting additional movements to the Neotropics, various parts of Oceania and southeast Asia. The production of thousands of dust-like, wind-dispersed, seeds by most lobeliads doubtless accounts for most of these long-distance dispersal events. Calibration of Antonelli's molecular phylogeny against fossils and various geologic milestones to form a timeline of lobeliad evolution (see also ) excludes continental drift as a possible explanation for these disjunctions. Fourth, based on an excellent sampling of genera and geographic regions occupied, Antonelli provides the first nearly complete view of geographic diversification across the family. A major finding is the SCBL clade (Siphocampylus, Centropogon, Burmeistera, Lysipomia), which comprises half the family and is endemic to the Neotropics. This clade is especially diverse in the northern Andes, which has undergone massive uplift over the past 10-20 million years and may, in so doing, have driven high rates of speciation in several other plant groups (for example, Espeletia, Fuchsia, Bromeliaceae: Tillandsioideae, Rubiaceae) [18–22]. The SCBL clade is embedded in a broader New World clade, including taxa from North America, the Caribbean, Central America and temperate Chile, as well as a few taxa representing long-distance dispersal events to the Pacific and Asia. This New World clade is sister to the clade consisting of the Old World woody lobeliads strong support for the latter confirms the clade sister to and including L. nicotianifolia found by Givnish et al. . Further investigation of the New World clade should pay rich dividends, given its extraordinary diversity of growth forms and geographic distributions, and what appear to be independent origins of the woody habit in the Caribbean (for example, L. portorescensis, L. vivaldii), temperate Chile (for example, L. polyphylla), and the montane Neotropics (for example, Burmeistera, Centropogon).
Finally, and surprisingly, Antonelli uses his phylogeny to argue that the giant woody lobeliads of Hawaii and East Africa are not examples of convergent evolution. This is, to me, a baffling claim - and yet one that Antonelli clearly feels is vitally important, given that 'testing' this claim forms the frame for his entire paper. This claim, I will now show, cannot be supported by the data and rationale provided.
There are four fundamental flaws in Antonelli's claim. First, his definition of convergence for giant lobeliads is overly restrictive and sets up a straw man:
'These results confidently show that lobelioid species commonly called "giant" are very closely related and have not developed their giant form from herbaceous ancestors independently. According to some early authors [Hedberg, Fries & Fries, Mabberley], convergence from herbaceous plants into tall treelets would have occurred independently in different mountain systems in response to similar tropical alpine climates consisting of nightly frosts and rapid temperature fluctuations.'
Why restrict convergence on the giant habit to those cases in which herbs were the immediate ancestors? Would convergence on that highly distinctive growth form be any less convergence if the ancestral form were not herbaceous, but some other life form instead? Obviously, no. One of the 'early' authors whom Antonelli cites is Mabberley . Not only does Mabberley not speak of an herbaceous ancestor, he outlines a hypothesis in which the ancestral taxa from which giant forms adapted to high elevations in the tropics are derived from less specialized woody species in which herbaceous species occasionally evolve from woody species and, most importantly, in which all African, Hawaiian and South Asian woody lobeliads are considered part of Lobelia section Rhychopetalum. More broadly, almost all authors positing specific ancestors for the Hawaiian lobeliads named only woody species (see ). In sum, Antonelli's artful restriction of convergence on the giant growth form to only those cases with different herbaceous ancestors is overly restrictive and logically unnecessary, and does not correspond to the historical use of the idea by most authors, including those actively working on the African and Hawaiian lobeliads today (see [14–16]). Antonelli, in using this inappropriate definition, also chose to ignore the conclusions of Mabberley, who had - in the absence of molecular data - pointed to the independent origins of giant lobeliads in Africa and Hawaii from closely related woody progenitors.
Second, Antonelli's phylogeny lacks sufficient resolution to evaluate whether giant species from Hawaii and Africa (or elsewhere) form a clade or not. While he found that woody species from Africa, South Asia, Polynesia, and the Bonin and Hawaiian Islands form a clade - consistent with findings by Givnish et al.  and Knox et al.  - Antonelli's phylogeny has a seven-way polytomy that prevents assessment of relationships among the different geographic groups and, for the African and Hawaiian taxa, of relationships within such groups. Claiming that the African and Hawaiian giant lobeliads are not convergent simply because they 'all derive from a single ancestor' is meaningless. All monocots share a single ancestor. However, does this mean that more than 20 apparent origins of fleshy fruits and of net venation  are not, in fact, independent? No. Among such origins are intercalated many groups with the capsular fruits and parallel venation ancestral to monocots, allowing the inference that monophyletic groups characterized by fleshy fruits or net venation represent independent origins. So, too, with woody lobeliads - only a minority of species have the giant growth form adapted to tropical alpine conditions, and detailed analyses of phylogenetic relationships within the Hawaiian taxa show that they are restricted to Lobelia sect. Galeatella and are embedded deep inside the Hawaiian clade, with non-giant woody species forming the remainder of that clade . Similarly, in East Africa the alpine lobelias with the most extreme giant-rosette growth-forms are embedded in a broader group containing less extreme forms . There is no doubt, given the description of the giant growth form by Antonelli, the specific species illustrated, and the thermal adaptive values he ascribes to the growth form, that he meant to restrict the usage of 'giant' to alpine and subalpine giant rosettes and not apply it more broadly to species with more slender stems, found in forests at lower elevations.
Third, it is misleading for Antonelli - in reconstructing ancestral character-states - to have overlaid all growth forms on the phylogeny except the very giant-rosette growth form whose independent origin(s) nominally are being assessed. Reconstruction of a nanophanerophyte (tree or treelet < 3 m tall) as the ancestor of the N4 clade says nothing about the distribution of origin(s) of the giant-rosette form within that clade. Overlaying the giant-rosette growth-form and reconstructing its ancestral occurrence is vital for any evaluation of evolutionary convergence.
Finally, in assessing the possibility of evolutionary convergence or stasis - of whether a particular trait has evolved independently in different lineages under similar ecological conditions, been maintained under such conditions and/or lost upon invasion of different conditions - it is equally vital to overlay such conditions on a phylogeny and reconstruct their ancestral states. This was not done by Antonelli, but should be considered best practice. Indeed, where possible, a formal analysis of correlated evolution of growth forms and environments should be conducted (for example, see ). Givnish et al.  showed that the ancestral environments of the giant species of Lobelia sect. Galeatella were alpine and subalpine bogs in Hawaii.
Thus, while Antonelli  has made fundamental contributions to our understanding of lobeliad evolution, I must take exception to his claim that African and Hawaiian giant lobeliads are not examples of convergent evolution. Manifestly, they are strikingly similar to the independently evolved species of Dendrosenecio in Africa, Espeletia in South America, and Argyroxiphium in Hawaii and both groups of giant lobeliads also represent independent origins from woody ancestors. All of these groups share a distinctive tropical-alpine climate, as well as several distinctive morphological traits. Many of the latter have been demonstrated to be of adaptive value in tropical-alpine climates. Therefore, the giant lobeliads represent examples - indeed, paradigmatic examples - of convergent evolution.
There remains the deeper question of whether origins judged independent, based on the preceding criteria, are truly independent. Might there be some developmental pathway or pattern of genetic variation in a broader lineage that makes the repeated origin of a particular trait more likely? Only detailed genetic studies can reveal whether the same genes and/or pathways are tapped in 'independent' origins. Such investigations have shown, for example, that melanic pelage has evolved in wholly different ways in rock pocket mice on black lava flows in Arizona versus New Mexico .
Future studies of lobeliad evolution could benefit from two new approaches that could foster research by the community as a whole. First, broad-scale phylogenetic studies should incorporate far more sequence data, to help resolve many of the very short branches in the lobeliad phylogeny (for example, those involving the divergences of the clades from Hawaii, Polynesia, the Bonin Islands and South Asia ). With next-generation DNA sequencing becoming cheaper and more powerful almost monthly, it should soon be possible to sequence whole-plastid genomes for scores of species. Eric Knox (personal communication) has such plans for several lobeliad genera and my colleagues and I hope to sequence plastomes for representatives of all Hawaiian genera in the immediate future. Second, it would be extremely helpful to sequence the entire genome of at least one lobeliad, to facilitate studies on the genetic basis for the extraordinary range of variation in several ecological significant traits seen across the family or in smaller groups (for example, fleshy fruits versus capsular fruits with wind-dispersed seeds succulent versus non-succulent stems insect- versus bird-pollinated flowers). A growing cadre of lobeliad ecologists and evolutionary biologists, and the broader evolutionary community, would greatly benefit from such studies.
Ophthalmosaurus and the Bottlenose Dolphin
You can't ask for two animals more separated in geologic time than Ophthalmosaurus and the bottlenose dolphin. The former was an ocean-dwelling ichthyosaur ("fish lizard") of the late Jurassic period, 150 million years ago, while the latter is an extant marine mammal. The important thing, though, is that dolphins and ichthyosaurs have similar lifestyles, and thus evolved similar anatomies: sleek, hydrodynamic, flippered bodies and long heads with extended snouts. However, one shouldn't oversell the similarity between these two animals: dolphins are among the most intelligent creatures on earth, while even the big-eyed Ophthalmosaurus would have been a D student of the Mesozoic Era.
Homoplasy and Convergent Evolution
In the last few posts in this series, we introduced the concept that individual characteristics (such as individual gene sequences) may not always match the phylogeny, or species tree for a group of related organisms. Incomplete lineage sorting is one way for this to occur, but another is for similarities to arise through independent events. Such features would have the superficial appearance of being inherited from a common ancestor, but in fact would be examples of homoplasies (singular = homoplasy): features shared between species that were not inherited from a common ancestor.
Birds of a feather
One classic example of a homoplasy is powered flight in birds and (some) mammals (i.e. bats). The species tree for birds, bats and non-flying mammals (for example, mice) places all mammals together as more closely related to each other than any is to birds. In order to explain the shared feature of powered flight for bats and birds, then, one needs to model it as a homoplasy – as independent events arising on two separate lineages:
The alternate explanation – that powered flight is homologous between bats and birds (and thus present in their last common ancestor) – would require that all mammals except for bats have lost this ability (to say nothing of the reams of DNA sequence data that support the above species tree). Beyond this evidence, there is also good reason from comparative anatomy to think that powered flight arose independently in bats and birds. Birds use feathers attached along the length of their forelimbs to provide lift. In contrast, bats use a membrane to form their wings, and this membrane is attached between their digits as well as to their body:
Both solutions work well, but when we break down the larger trait of “powered flight” into its component parts, we see that though the trait as a whole is convergent, the underlying components are not. This observation further supports the conclusion that powered flight in birds and mammals arose separately.
Homoplasy vs. homology
We can illustrate an example of how a simple DNA sequence homoplasy arises using a phylogeny. Suppose three species have the following sequence for a portion of the same gene:
Based on these data alone, the simplest (most parsimonious) phylogeny would be as follows:
Based on these data, the ancestral sequence would be inferred to be “TCATCC”, and the branch of the phylogeny leading to Species A would have one mutation to explain the observed sequence difference. In the absence of other evidence, this phylogeny would be the best fit for the data.
This tidy picture, however, could be upset by more data – data that demonstrates that the simple species tree we have drawn above is in fact incorrect. If so, then we need to fit the above sequences into a different species tree – meaning that we will need to explain the pattern using more than one mutation event. Let’s work through a hypothetical example to show the process.
Let’s suppose that sequence data for several hundred additional genes are compared for these three species, as well as for a number of other related species not shown in our species tree. Let’s also suppose that these data strongly support a different species tree than the one we just generated – in the vast, vast majority of cases, the data supports a tree with Species A and B as closest relatives, with Species C as more distantly related. This would “force” us to redraw the species tree as follows, placing our original short sequences into a different pattern along with their species:
Let’s also suppose that the DNA sequence data for this particular gene sequence from the additional species not shown on the species tree indicate that the ancestral sequence actually had a “T” in the second position rather than a “C”:
Now we have to account for all three species in our species tree having a non-ancestral sequence at the second position, as well as try to make sense of the mutation events that led to the pattern we see here. Note that we are still constrained to make the most parsimonious explanation for the whole of the data, but for this particular gene, we are forced to invoke multiple mutation events to fit the pattern to the species tree. We make this choice, however, because it would be even more unlikely for multiple mutation events to have shaped the pattern of the hundreds of other gene sequences in a coordinated fashion – and those other sequences support this version of the species tree.
If you take the time to try “solving” the gene tree by adding mutation events to the species tree you’ll soon realize that at least three mutation events are needed to produce the observed pattern. There are also solutions that use more than three mutation events, but they are less likely explanations. One of the possible solutions is shown below:
In the branch of the phylogeny leading to Species A and Species B, a (T to G) mutation occurs prior to the A / B divergence (represented by the red bar). A second mutation then occurs on the lineage leading to Species B that changes the G at the same position to a C (represented with a blue bar). Independently, the lineage leading to Species C also has a mutation at this position, changing the ancestral T to a C (also represented with a blue bar). The end result is that two of the sequences (in Species B and C) have become identical – but neither inherited the “C” at the second position from their common ancestor. In other words, they have arrived at the same “destination” from different starting points, or “converged” on a common sequence. Not surprisingly, this phenomenon is known as convergent evolution. For these two species, the “C” at the second position is not homologous (a similarity inherited from a common ancestor), but rather a homoplasy – a similarity that resulted from independent events on two lineages.
Homoplasies can be as simple as single DNA monomer changes (as in this example), or as complex as the independent reorganization of multiple systems with numerous genes and body parts to converge on a solution (as in the case for powered flight in birds and bats). In both cases, however, we can determine that they arose as independent events on separate lineages because these features do not fit onto the species tree as unique events.
The power of convergence
Since homoplasies act as markers that flag repeated evolutionary events, looking for homoplasies in species trees is a useful way to test hypotheses about the reproducibility of evolution, or how often species converge on similar solutions. As it turns out, evolution is remarkably repeatable for many general traits. There are numerous examples of repeated, independent innovations over evolutionary history, some of which we will examine in more detail in upcoming posts:
- Streamlined body shape: the streamlined body form of aquatic life such as fish, ichthyosaurs, whales, seals and diving birds (e.g. penguins) are all independent, convergent adaptations to an aquatic lifestyle.
- Powered flight: in addition to birds and bats, powered flight also evolved independently in insects and pterodactyls.
- Echolocation: some mammals, such as bats and whales, have independently developed systems that allow them to locate food through detecting how sound that they generate echoes off structures and prey in their environment.
- Camera eyes: the repeated evolution of camera eyes (i.e. eyes that use a lens) is one of the most striking examples of convergent evolution. Camera eyes have independently evolved in cnidarians (certain jellyfish), cephalopods (such as squid and octopus) and vertebrates (birds, mammals).
One thing to note is that these widespread examples of convergence are all shaped by the physical environment of the organisms in question – the perception of light (eyes), the ability to fly through air (wings), or move efficiently through water (streamlined body). The fixed presence of these environmental features would be expected to shape the adaptation of many species.
Previously, we introduced the concept of a homoplasy – a similarity in form in two lineages that arises due to independent events. In the example we looked at last time, birds and bats independently obtained powered flight through convergent evolution – with bats arriving at membrane-based wings, and birds at feather-based wings. Since the last common ancestral population for bats and birds was a species that did not have powered flight, this is a good example of a homoplasy – one that arose through convergent evolution.
Underneath this convergent event, however, there is a deeper connection. Bats and birds are both tetrapods – organisms with backbones and four limbs. The tetrapod body plan was already a feature of their last common ancestral population, and has been maintained in both lineages. As such, when considered strictly as a forelimb, bat wings and bird wings are homologous structures. In birds and bats, forelimbs have been shaped through natural selection for flight in different ways, but the starting point for both was a homologous structure. In other words, underneath the convergent event of powered flight in bats and birds is a deeper homology – the limb upon which both lineages independently constructed a wing. To represent this on a phylogeny, we would place the tetrapod body plan prior to the divergence of all tetrapods, and powered flight as two events on the appropriate lineages:
This pattern – convergent events with deeper homologies lurking beneath them – is one that is seen time and again in evolution. In fact, these deeper homologies improve the odds that convergent events will occur, since they provide a common basis that separate lineages can use for independent innovation. For bats and birds, adaptations leading to flight were possible because both lineages had forelimbs that could be modified, over time, from one function to another. While this example is at the anatomical level, these sorts of “predispositions” and the convergent events that arise from them can be observed at the molecular level as well.
The eyes have it
As we mentioned in the previous post in this series, camera eyes are one of the most striking examples of convergent evolution, having appeared independently in several lineages (the most common examples of which are vertebrates, cephalopods such as octopus and squid, and certain jellyfish). Camera eyes have a light-sensitive cell layer (the retina) as well as a lens that focuses light on the retina. Explaining the distribution of camera eyes among these three groups requires us to invoke three convergent events on their phylogeny (“cnidarians” are the group in which jellyfish are found):
At first glance, it seems wildly improbable that three distantly-related lineages would independently converge on such a remarkable structure as a camera eye. As it turns out, however, a key homology between all three groups greatly improved those odds – the molecules that act as light sensors.
At its most basic form, sensing of the external environment requires that the environment induce a change within cells. Accordingly, sensing light requires a light-induced change of some kind. The key molecules that perform this function in all three of the above groups are proteins called opsins and their chemical partners (a group of compounds called retinals). Each opsin protein has a retinal attached to it, and together the opsin/retinal pair acts as a light sensor. Retinals change their shape when they interact with light (i.e. absorb a photon, represented by the gamma in the diagram below). This shape change in turn alters the shape of the opsin protein attached to the retinal:
The change in shape of the opsin protein affects the flow of electrical charge in the cells responsible for sensing light, and these changes in electrical charge are what are perceived and interpreted by the brain as “light.”
The opsin/retinal system of detecting light is a very widespread system – in fact, all animals that can detect light use these molecules as the physical basis for doing so, whether they have camera eyes or other eye types (such as compound eyes, or merely patches of light-sensitive cells). This is strong evidence that the opsin / retinal system predates the divergence of the three groups we are considering:
With this knowledge in hand, we can see that the development of camera eyes in these lineages is not as improbable as we might have thought at first. In all three cases, these lineages built a camera eye around a preexisting molecular system for detecting light. The camera eyes themselves might be convergent, but they are based on a deeper underlying homology that improved the odds that they would appear through successive modifications of an ancestral system. And as we saw for bird and bat wings, there are differences between the camera eyes in these lineages that support the hypothesis that they are the result of convergent events (the most well-known example of which is that the vertebrate and cephalopod eyes have their nerve “wiring” in opposite orientations).
Hearing is believing
A second example of “molecular predisposition” leading to convergence can be seen in the molecular machinery underlying a different form of sensory perception – the ultrasonic hearing required for echolocation in bats and toothed whales. Both groups use highly tuned echolocation for navigation and seeking prey in an environment where visual perception is limited or lacking altogether. The evidence that the development of echolocation in these two very divergent groups of mammals is due to convergent evolution is strong – no other mammals more closely related to either group has such an ability.
The cellular / molecular basis for detecting sound in mammals is a set of cells in the ear that extend hair-like projections (called cilia) that vibrate in response to different wavelengths of sound. Cilia also change their length and vibratory properties in response to different auditory stimuli. The vibrations are used to change the flow of electrical charge in these cells, eventually leading to nervous system signals that the brain perceives as sound. All mammals use a protein called prestin as part of the auditory system. Prestin is a “motor protein” that can change cell shape by moving internal structures around – and mammals use it for modifying cilia in response to sound.
The cilia/prestin system is known to predate all mammals, so it is not surprising that toothed whales and bats use this system for hearing. What is interesting, however, is that in these groups the prestin protein has been independently shaped through natural selection to be tuned to high frequency (ultrasonic) sound more useful for echolocation. In fact, in a phylogeny restricted to prestin sequences, bat prestins and toothed whale prestins appear to be the most closely related to each other – a finding wildly at odds with the species tree for bats and whales. Further examination, however, shows that these striking similarities are the result of convergent evolution, not a more recent shared ancestry. In both cases, the prestin protein was available to become attuned to ultrasonic wavelengths, and similar (though not identical) mutation events in both lineages were selected for along the way – an additional example of a “deep homology” favoring independent convergent events.
Summing up: evolution as a non-random process
One common misconception I encounter about evolution is that it is predominantly a random process – one that is mainly influenced by chance events. While we have already shown that evolution has a strongly non-random component (natural selection), this discussion of convergent evolution further demonstrates that evolution is repeatable in certain important ways. When natural selection affects distantly-related groups in a similar fashion, we often observe similar outcomes. These similar outcomes are in many cases favored by prior history (homology) and arrived at through similar, but not identical paths (demonstrating that contingency and chance are present as well). Evolution is thus a balance of contingent events (mutations and other chance events) and emphatically non-contingent events (selection, convergent evolution).
In the next post in this series, we’ll return to bat echolocation to explore how evolution of one species can be greatly shaped by another species in close relationship with it – a phenomenon known as coevolution.
Convergent evolution of a complex fruit structure in the tribe Brassiceae (Brassicaceae)
PREMISE OF STUDY: Many angiosperms have fruit morphologies that result in seeds from the same plant having different dispersal capabilities. A prime example is found in the Brassiceae (Brassicaceae), which has many members with segmented or heteroarthrocarpic fruits. Since only 40% of the genera are heteroarthrocarpic, this tribe provides an opportunity to study the evolution of an ecologically significant novelty and its variants. METHODS: We analyzed nuclear (PHYA) and plastid (matK) sequences from 66 accessions using maximum parsimony, maximum likelihood, and Bayesian inference approaches. The evolution of heteroarthrocarpy and its variants was evaluated using maximum parsimony and maximum likelihood ancestral state reconstructions. KEY RESULTS: Although nuclear and plastid phylogenies are incongruent with each other, the following findings are consistent: (1) Cakile, Crambe, Vella, and Zilla lineages are monophyletic (2) the Nigra lineage is not monophyletic and (3) within the Cakile clade, Cakile, Didesmus, and Erucaria are paraphyletic. Despite differences in the matK and PHYA topologies at both deep and shallow nodes, similar patterns of morphological evolution emerge. Heteroarthrocarpy, a complex morphological trait, has evolved multiple times across the tribe. Moreover, there are convergent transitions in dehiscence capabilities and fruit disarticulation across the tribe. CONCLUSIONS: We present the first explicit analysis of fruit evolution within the Brassiceae, which exemplifies evolutionary lability. The repeated loss and gain of segment dehiscence and disarticulation suggests conservation in the genetic pathway controlling abscission with differential expression across taxa. This study provides a strong foundation for future studies of mechanisms underlying variation in dispersal capabilities of Brassiceae.
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Functional Convergence: Distinct Enzyme Lineages Producing Similar Compounds
The monoterpene alcohol linalool is present in the floral scent of many species. Its diverse ecological functions have recently been reviewed (Raguso, 2016a). This compound may be both an attractant for pollinators (in orchids for example) and a repellant for various herbivores. Emission of linalool by N. attenuata leaves has been proposed to attract predators of the generalist herbivore Manduca sexta (He et al., 2019). When present in nectar, it could contribute to avoid microbe proliferation. Two enantiomeric forms of this molecule exist: (/?)-(—)-linalool and (S)-(+)-linalool. Both forms have distinct biochemical properties and impacts on insects. For instance, female moths oviposit more on Datura wrightii plants emitting (S)-(+)-linalool over control plants, while plants emitting (/?)-(—)-linalool are less preferred than control plants (Reisenman et al., 2010). Since the first characterization of C. breweri linalool synthase (Dudareva et al., 1996), TPSs able to catalyze the formation of linalool from GPP have been functionally characterized in many plant species, including A. thaliana (Ginglinger et al., 2013), F. x ananassa (Aharoni et al., 2004), and Rosa genus (Magnard et al., 2018). Phylogenetic analysis indicates that these genes belong to four TPS subfamilies (Figure 12.2). For example, in R. chinensis, three genes encoding potentially functional TPSs are expressed in petals, RcLINS, RcLIN-NERSl, and RcLIN-NERS2. The LIN-NERS1/2 genes are clustered on chromosome 5 of the rose genome (Raymond et al., 2018) whereas RcLINS gene is on chromosome 2. RcLINS is responsible for the small amounts of (/?)-(—)-linalool present in rose scent (Magnard et al., 2018). RcLIN-NERSl, and RcLIN-NERS2 genes, although weakly expressed, are probably not active in planta as neither nerolidol, nor (S)-(+)-linalool are present in rose petals. A comparison of roses with strawberries, show that these two members of the Rosaceae family have evolved different enzymes to produce linalool. F. x ananassa uses the (S)-(+)-linalool /nerolidol synthase FaNESl (Aharoni et al., 2004), whereas the orthologous RcLIN-NERS2 is ineffective in rose flowers. Conversely, the small quantity of linalool produced in rose flowers derives from the activity of the RcLINS (/?)-(—(-linalool synthase, which is unable to produce nerolidol. More generally, linalool or linalool/nerolidol synthase activities are well correlated with their belonging to a specific TPS subfamily (Figure 12.2). Monofunctional linalool synthases cluster into the TPS-b subfamily. Like RcLINS, most of these b class enzymes with linalool synthase activity generally produce (/?)-(—)-linalool. The bifunctional linalool/nerolidol synthases, including RcLIN-NERSl and RcLIN-NERS2 belong to the TPS-g subgroup together with some linalool/nerolidol/geranyllinalool
FIGURE 12.2 Diversity of linalool synthases characterized from different plant species. Unrooted Neighbor Joining tree depicting the classification of linalool synthases and linalool/nerolidol synthases from plants into terpene synthase (TPS) subfamilies. Linalool/nerolidol/geranyllinalool synthases were also included. Protein sequences were aligned with ClustalW and tree was constructed using Geneious software. Linalool isomers are indicated by colors of the GenBank accession letters. Black letters, unidentified linalool isomer blue letters (R)-(-)-linalool synthase orange letters (Л/SJ-linalool synthase (racemic) pink letters (5)-(+)-linalool synthase.
synthases. The linalool isomer produced by synthases belonging to this group is usually (£)-(+)- linalool, like RcLIN-NERSl and 2. Although not all studies report the linalool enantiomer that is produced by the different species, the general trend is that (S)-(+)- and (/()-(-)-!inalool synthases have evolved independently, probably under the selection pressures exerted by both herbivores and pollinators.
Another example of convergent evolution is the biosynthesis of phenylpropenes. These compounds are phenylpropanoids derived from phenylalanine, which participate in the unique aroma of many fruits, herbs and spices. In flowers, they attract pollinators and may be used as defense compounds against fungi and bacteria. Many plants synthesize volatile phenylpropenes in their floral and vegetative organs as a defense against insect pests and herbivores. For example, the stamens of roses emit eugenol (Yan et al., 2018). The last step of the biosynthesis pathway to eugenol and isoeugenol is performed by the NADPH-dependent reductases eugenol synthase and isoeugenol synthase, which catalyze the elimination of an acyl moiety from coniferyl acetate (reviewed in Koeduka, 2014). Phenylpropene synthases belong to the PIP family of reductases and are distributed in two distinct protein lineages in C. breweri and P. x hybrida (Koeduka et al., 2008), suggesting independent evolutionary origins. These independent origins have since been supported by studies in a number of other plants such as F. x ananassa and Daucus carota (Aragiiez et al., 2013 Yahyaa et al., 2019).
Convergent and Parallel Evolution
There must be a distinction between resemblances due to propinquity of descent and those due solely to the similarity of function. As previously discussed in the section The Evidence for Evolution: Harmony refers to structural similarities or the correspondence of features in different organisms due to inheritance from a common ancestor. Humans, whales, dogs, and bats all have homologous forelimbs. Because they share a common ancestor with similarly arranged forelimbs, the skeletons of these limbs are all made up of bones arranged in the same pattern.
Analogy refers to the correspondence of features due to the similarity of function that is not related to common descent. The wings of birds and flies are similar. Their wings are not modified versions of structures that existed in a common ancestor but instead evolved independently as adaptations to a common function, flying. The similarities between bat and bird wings are partly homologous and partly analogous. Their skeletal structure is homologous due to common descent from a reptilian ancestor's forelimb however, the modifications for flying are distinct and independently evolved, and they are analogous in this regard.
Convergent features are those that become more similar rather than less similar as a result of independent evolution. Convergence is frequently associated with functional similarities, such as the evolution of wings in birds, bats, and flies. The external morphology of the shark (a fish) and the dolphin (a mammal) is very similar their similarities are due to convergence, as they evolved independently as adaptations to aquatic life.
What is Parallel Evolution?
Parallel evolution is another term used by taxonomists. Parallelism and convergence aren't always easy to tell apart. Convergent evolution occurs when descendants resemble each other more than their ancestors did in terms of some feature. Parallel evolution implies that two or more lineages changed in similar ways so that the evolved descendants are as similar as their ancestors were. The evolution of marsupials in Australia, for example, paralleled the evolution of placental mammals in other parts of the world.. There are marsupials in Australia that look like wolves, cats, mice, squirrels, moles, groundhogs, and anteaters.
Because of their adaptation to similar ways of life, these placental mammals and the corresponding Australian marsupials evolved independently but in parallel lines. The similarities between a true anteater (genus Myrmecophaga) and a marsupial anteater (Myrmecobius) stem from homology—both are mammals. Others are similar in that they both feed on ants.
Parallel and Convergent Evolution
The independent evolution of similar traits in different but equivalent habitats is referred to as parallel evolution. It can be found in habitats that are geographically separated but otherwise equivalent. Parallel evolution results in morphological similarities between two species. Because the environmental influences on the species are similar, both unrelated and distantly related species may undergo parallel evolution in equivalent habitats. The figure below depicts various evolutionary patterns.
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Australia's marsupial mammals, which are similar to other placental mammals, are an example of parallel evolution. Marsupial mammals include the wolf, mole, mice, rat, and others. Another example of parallel evolution is the evolution of old and new world monkeys. A long time ago, both old and new world monkeys shared a common ancestor. Despite being separated by the Atlantic Ocean, old and new world monkeys evolve in very similar ways.
What is Convergent Evolution?
The independent evolution of analogous structures in unrelated species is referred to as convergent evolution. It happens when unrelated species coexist in the same environment. As an adaptation to a similar environmental pressure, convergent evolution gives rise to analogous traits in unrelated species. Though the anatomical structure of analogous traits differs, they are functionally similar. For example, despite the fact that North American cactuses (family Cactaceae) and South African euphorbias (family Euphorbiaceae) are from different families, both have thick stems and are succulent as an adaptation to survive in desert regions. The Cactaceae and Euphorbiaceae families are depicted below.
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Another example of convergent evolution is the emergence of wings as an adaptation to flight in birds, bats, and insects. Dolphins and sharks' body shapes have also evolved as a result of convergent evolution.
Despite the fact that dolphins and sharks are distantly related, their body shapes are adapted for fast swimming. As a result, the environment forces distantly related organisms' phenotypes to become analogous. Another example of convergent evolution is the evolution of the eye in vertebrates, cephalopods, and cnidarians. The formation of analogous structures is known as homoplasy.
Similarities Between Parallel and Convergent Evolution
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Evolutionary patterns are classified into two types: parallel evolution and convergent evolution.
In different species, parallel and convergent evolution occur independently.
Under the influence of the same environmental pressures, both parallel and convergent evolution occurs.
Neither parallel nor convergent evolution results in speciation.
Difference Between Parallel and Convergent Evolution
Parallel Evolution: The independent evolution of similar traits in different but equivalent habitats is referred to as parallel evolution.
Convergent Evolution: The independent evolution of analogous structures in unrelated species is referred to as convergent evolution.
Parallel Evolution: Parallel evolution occurs in habitats that are different but equivalent.
Convergent Evolution: Convergent evolution takes place within a specific habitat.
Parallel Evolution: In parallel evolution, two distinct species evolve independently while maintaining the same level of similarity.
Convergent Evolution: In convergent evolution, two distinct species evolve analogous traits.
Convergent Evolution: Convergent evolution occurs in species that are not related.
Parallel Evolution: An example of parallel evolution is the evolution of old and new world monkeys.
Convergent Evolution: An example of convergent evolution is the development of the eye in vertebrates, cephalopods, and cnidarians.
Review papers and textbooks, such as Futuyma 2013 tend to focus on how one can identify convergent evolution and on presenting particularly compelling examples of convergence or lack thereof. A few authors have attempted to make broad generalizations based on these observations. Gould 1990 argues that evolution is dominated by historical contingency, while Conway Morris 2004 (see also papers in Conway Morris 2008) and McGee 2011 argue that convergence is ubiquitous. Conway Morris 2004 argues for both adaptive and constraint-based mechanisms for convergence, while McGee 2011 leans most heavily on constraints as a mechanism. Losos 2011 is a nice early-21st-century review paper that carefully describes what we can (and cannot) learn from studies of convergent evolution.
Conway Morris, Simon. 2004. Life’s solution: Inevitable humans in a lonely universe. Cambridge, UK: Cambridge Univ. Press.
This book catalogues convergent evolution across a wide range of taxa and time scales. Conway Morris argues that convergence is common and that the universe is predictable—even going so far as to argue for the inevitability of the evolution of our own species.
Conway Morris, Simon, ed. 2008. The deep structure of biology: Is convergence sufficiently ubiquitous to give a directional signal? West Conshohocken, PA: Templeton Foundation.
This edited volume includes chapters on a wide range of topics in convergent evolution, including both empirical results and philosophical considerations.
Futuyma, Douglas J. 2013. Evolution. Sunderland, MA: Sinauer.
This now-classic textbook discusses convergent evolution explicitly in Chapter 3 (Patterns of Evolution), but the topic also appears in several other contexts and chapters.
Gould, Steven J. 1990. Wonderful life: The Burgess Shale and the nature of history. New York: W. W. Norton.
Gould’s classic book uses the Burgess Shale—a fossil field with exceptional preservation of the soft body parts of an astounding assortment of middle Cambrian fossils—as an argument in favor of the role of chance and contingency in evolution.
Losos, Jonathan B. 2011. Convergence, adaptation, and constraint. Evolution 65:1827–1840.
An excellent review focusing on what we can (and cannot) conclude from examples of convergent evolution. Losos argues that other forms of evidence (beyond phenotypic similarity) are needed to distinguish adaptive convergence from convergence due to genetic or developmental constraint.
McGee, George. 2011. Convergent evolution: Limited forms most beautiful. Cambridge, MA: MIT Press.
McGee reviews a multitude of examples of convergent evolution, from genes to phenotypes to behavior, and argues that the ubiquity of convergent evolution is mainly due to functional and developmental constraints.
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