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Evolutionary tradeoffs, Pareto optimality and the morphology of ammonite shells.

Tendler A, Mayo A, Alon U - BMC Syst Biol (2015)

Bottom Line: After mass extinctions, surviving species evolve to refill essentially the same pyramid, suggesting that the tasks are unchanging.We infer putative tasks for each archetype, related to economy of shell material, rapid shell growth, hydrodynamics and compactness.These results support Pareto optimality theory as an approach to study evolutionary tradeoffs, and demonstrate how this approach can be used to infer the putative tasks that may shape the natural selection of phenotypes.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular cell biology, Weizmann Institute of Science, Rehovot, 76100, Israel. tendlea@gmail.com.

ABSTRACT

Background: Organisms that need to perform multiple tasks face a fundamental tradeoff: no design can be optimal at all tasks at once. Recent theory based on Pareto optimality showed that such tradeoffs lead to a highly defined range of phenotypes, which lie in low-dimensional polyhedra in the space of traits. The vertices of these polyhedra are called archetypes- the phenotypes that are optimal at a single task. To rigorously test this theory requires measurements of thousands of species over hundreds of millions of years of evolution. Ammonoid fossil shells provide an excellent model system for this purpose. Ammonoids have a well-defined geometry that can be parameterized using three dimensionless features of their logarithmic-spiral-shaped shells. Their evolutionary history includes repeated mass extinctions.

Results: We find that ammonoids fill out a pyramid in morphospace, suggesting five specific tasks - one for each vertex of the pyramid. After mass extinctions, surviving species evolve to refill essentially the same pyramid, suggesting that the tasks are unchanging. We infer putative tasks for each archetype, related to economy of shell material, rapid shell growth, hydrodynamics and compactness.

Conclusions: These results support Pareto optimality theory as an approach to study evolutionary tradeoffs, and demonstrate how this approach can be used to infer the putative tasks that may shape the natural selection of phenotypes.

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Related in: MedlinePlus

Ammonoids repeatedly filled the same triangle in D-W plane after mass extinctions. (A) All of the ammonoid data used in the present study. Red points are genera before the FF (first) mass extinction, genera after FF are denoted by blue points. The green curve is W = 1/D. (B) Ammonoids before the FF extinction, together with a schematic arrow for the direction of evolution from ancestral taxa. (C) Genera between FF and DM mass extinctions fill out a triangle (obtained by applying the SISAL algorithm [41] on the dataset), surviving genera from the FF mass extinction are denoted by red bold points. (D) Ammonoids between DM and PT mass extinctions fill a triangle, surviving genera from the DM mass extinction are denoted by red bold points. (E) Ammonoids after the PT mass extinction fill a triangle, surviving genera from the PT mass extinction are denoted by red bold points. (F) Ammonoids from different periods, together, genera between FF and DM are denoted blue, DM to PT in red and post PT in green. The shell morphologies of the three archetypes at the vertices of the triangle are shown.
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Fig3: Ammonoids repeatedly filled the same triangle in D-W plane after mass extinctions. (A) All of the ammonoid data used in the present study. Red points are genera before the FF (first) mass extinction, genera after FF are denoted by blue points. The green curve is W = 1/D. (B) Ammonoids before the FF extinction, together with a schematic arrow for the direction of evolution from ancestral taxa. (C) Genera between FF and DM mass extinctions fill out a triangle (obtained by applying the SISAL algorithm [41] on the dataset), surviving genera from the FF mass extinction are denoted by red bold points. (D) Ammonoids between DM and PT mass extinctions fill a triangle, surviving genera from the DM mass extinction are denoted by red bold points. (E) Ammonoids after the PT mass extinction fill a triangle, surviving genera from the PT mass extinction are denoted by red bold points. (F) Ammonoids from different periods, together, genera between FF and DM are denoted blue, DM to PT in red and post PT in green. The shell morphologies of the three archetypes at the vertices of the triangle are shown.

Mentions: Plotting each genus of ammonoids as a point in this morphospace, ignoring coiling axis changes, Raup discovered that most of the theoretical morphospace is empty: many possible shell forms are not found. The existing forms lie in a roughly triangular region in the W-D plane (Figure 3A). One reason for this distribution is geometric constraints. Researchers have suggested that ammonoids tend to lie to the left of the hyperbola W = 1/D [15,26], because beyond this curve shells are gyroconic (shells with non-overlapping whorls) (Figure 3A upper right corner). Such gyroconic shells are mechanically weaker and less hydrodynamically favorable [35,36]. It is noteworthy, however, that shells to the right of the curve do exist in nature, for example in the Bactritida or Orthocerida lineages, which are probably ancestral to the ammonoids (Figure 3B, top right) [37-40], as well as in heteromorph ammonoids that occasionally occur in the Mesozoic and more commonly in the Cretaceous. Thus the W = 1/D curve is unlikely to be an absolute geometric constraint (for more evidence, see Additional file 1).Figure 3


Evolutionary tradeoffs, Pareto optimality and the morphology of ammonite shells.

Tendler A, Mayo A, Alon U - BMC Syst Biol (2015)

Ammonoids repeatedly filled the same triangle in D-W plane after mass extinctions. (A) All of the ammonoid data used in the present study. Red points are genera before the FF (first) mass extinction, genera after FF are denoted by blue points. The green curve is W = 1/D. (B) Ammonoids before the FF extinction, together with a schematic arrow for the direction of evolution from ancestral taxa. (C) Genera between FF and DM mass extinctions fill out a triangle (obtained by applying the SISAL algorithm [41] on the dataset), surviving genera from the FF mass extinction are denoted by red bold points. (D) Ammonoids between DM and PT mass extinctions fill a triangle, surviving genera from the DM mass extinction are denoted by red bold points. (E) Ammonoids after the PT mass extinction fill a triangle, surviving genera from the PT mass extinction are denoted by red bold points. (F) Ammonoids from different periods, together, genera between FF and DM are denoted blue, DM to PT in red and post PT in green. The shell morphologies of the three archetypes at the vertices of the triangle are shown.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4404009&req=5

Fig3: Ammonoids repeatedly filled the same triangle in D-W plane after mass extinctions. (A) All of the ammonoid data used in the present study. Red points are genera before the FF (first) mass extinction, genera after FF are denoted by blue points. The green curve is W = 1/D. (B) Ammonoids before the FF extinction, together with a schematic arrow for the direction of evolution from ancestral taxa. (C) Genera between FF and DM mass extinctions fill out a triangle (obtained by applying the SISAL algorithm [41] on the dataset), surviving genera from the FF mass extinction are denoted by red bold points. (D) Ammonoids between DM and PT mass extinctions fill a triangle, surviving genera from the DM mass extinction are denoted by red bold points. (E) Ammonoids after the PT mass extinction fill a triangle, surviving genera from the PT mass extinction are denoted by red bold points. (F) Ammonoids from different periods, together, genera between FF and DM are denoted blue, DM to PT in red and post PT in green. The shell morphologies of the three archetypes at the vertices of the triangle are shown.
Mentions: Plotting each genus of ammonoids as a point in this morphospace, ignoring coiling axis changes, Raup discovered that most of the theoretical morphospace is empty: many possible shell forms are not found. The existing forms lie in a roughly triangular region in the W-D plane (Figure 3A). One reason for this distribution is geometric constraints. Researchers have suggested that ammonoids tend to lie to the left of the hyperbola W = 1/D [15,26], because beyond this curve shells are gyroconic (shells with non-overlapping whorls) (Figure 3A upper right corner). Such gyroconic shells are mechanically weaker and less hydrodynamically favorable [35,36]. It is noteworthy, however, that shells to the right of the curve do exist in nature, for example in the Bactritida or Orthocerida lineages, which are probably ancestral to the ammonoids (Figure 3B, top right) [37-40], as well as in heteromorph ammonoids that occasionally occur in the Mesozoic and more commonly in the Cretaceous. Thus the W = 1/D curve is unlikely to be an absolute geometric constraint (for more evidence, see Additional file 1).Figure 3

Bottom Line: After mass extinctions, surviving species evolve to refill essentially the same pyramid, suggesting that the tasks are unchanging.We infer putative tasks for each archetype, related to economy of shell material, rapid shell growth, hydrodynamics and compactness.These results support Pareto optimality theory as an approach to study evolutionary tradeoffs, and demonstrate how this approach can be used to infer the putative tasks that may shape the natural selection of phenotypes.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular cell biology, Weizmann Institute of Science, Rehovot, 76100, Israel. tendlea@gmail.com.

ABSTRACT

Background: Organisms that need to perform multiple tasks face a fundamental tradeoff: no design can be optimal at all tasks at once. Recent theory based on Pareto optimality showed that such tradeoffs lead to a highly defined range of phenotypes, which lie in low-dimensional polyhedra in the space of traits. The vertices of these polyhedra are called archetypes- the phenotypes that are optimal at a single task. To rigorously test this theory requires measurements of thousands of species over hundreds of millions of years of evolution. Ammonoid fossil shells provide an excellent model system for this purpose. Ammonoids have a well-defined geometry that can be parameterized using three dimensionless features of their logarithmic-spiral-shaped shells. Their evolutionary history includes repeated mass extinctions.

Results: We find that ammonoids fill out a pyramid in morphospace, suggesting five specific tasks - one for each vertex of the pyramid. After mass extinctions, surviving species evolve to refill essentially the same pyramid, suggesting that the tasks are unchanging. We infer putative tasks for each archetype, related to economy of shell material, rapid shell growth, hydrodynamics and compactness.

Conclusions: These results support Pareto optimality theory as an approach to study evolutionary tradeoffs, and demonstrate how this approach can be used to infer the putative tasks that may shape the natural selection of phenotypes.

Show MeSH
Related in: MedlinePlus