Is Robust Image Formation a Key Innovation?

1
Is Robust Image Formation a Key Innovation?

• Predictability and Contingency in Macroevolution

2
vs.

• Predictability versus Contingency in
  Macroevolution
• How likely are certain key actualized adaptations
  to re-emerge, if we re-ran the tape of life, or
  if life evolved on other worlds?
• What are Good Tricks in design space (sensu
  Dennett, 1995)?
• Good Tricks must be more than just
  adaptationsthey must be key adaptations, likely
  to evolve iteratively and to have substantial
  macroevolutionary effects.
• Dennett (95), Dawkins (04), and Conway Morris
  (03) have all suggested that vision is an
  excellent candidate for Good Trick-hood
• Galis (01) Zuker (94) and Land Fernald (92)
  suggest vision may be key innovation
• Question Presented Here How predictable and / or
  contingent is the evolution of Vision and other
  forms of Robust Image Formation?
• Do these complex adaptive solutions represent key
  innovations?

3
What Do I Mean By Robust Image Formation?

• Robust Image is one which represents the
  detailed, three-dimensional topography of an
  organisms surrounding environment, including the
  spatial arrangement of objects and object
  features, shapes, textures, depths and distances.
  
• Physical Image of an object or stimulus is a
  functional category that applies to the
  distribution of a stimulus on a sensory receptor
  surface
• The stimulus ultimately projected onto the
  senso-receptor array may be chemical (as in
  olfaction) or energetic (as in vision,
  echolocation, and electrogeneration).
• However, only energetic stimuli provide enough
  information about the environment for an organism
  to form what I call a robust image
• Moreover, apart from vision (which is passive)
  only active energetic image-formation (pulse
  emission) is adequate for the task

4
What is a Key Innovation?

• Mayr (1963) and Simpson (1953) certain
  morphological, physiological, or functional
  complexes play a more significant role than
  others in directing particular macroevolutionary
  trajectories
• Associated with the origins of higher taxa
• Presumably by enabling the anointed lineage to
  occupy a new adaptive zone with reduced predation
  pressures (Van Valen, 1970)
• Measures
• Diversity
• Disparity
• Sister Taxa Comparisons vs. Tree Thinking
• Ecological Implications For Other Lineages
• Convergent (Iterative) Evolution a Statistical
  Bonus (re-run of tape)

5
Iterative Evolution of Camera-Type Eyes

• Camera-type eyes have evolved independently in 5
  phyla, including molluska, chordata, annelida,
  cnidaria, and arthropoda

6
Iterative Evolution of Compound Eyes

• The compound eye has also evolved independently
  in up to 4 phyla, including arthropoda (multiple
  times), annelida, molluska, and the echinoids
  (maybe)

7
Image-Forming Eyes and Diversification An
Empirical Investigation

• Land and Fernalds (1992) Claim 96!!!
• Although the convergent origin of the macroscopic
  arrangements of image-forming eyes occurred in
  only a handful of the 33 recognized metazoan
  phyla, these few eye-bearing phylanamely,
  Cnidaria, Molluska, Annelida, Arthropoda, and
  Chordataaccount for over 96 of the known
  species (Land Fernald, 1992).
• Isnt this strongly suggestive that vision is a
  key innovation? (No)
• Problems with the claim
• First, 3 of the phyla they mention (Cnidaria,
  Annelida, and Molluska) contain predominantly
  eye-less species, and hence including those
  entire phyla in the 96 count is misleading.
• Secondly, 2 clades with image-forming eyesnamely
  the arthropods and vertebratesaccount for the
  overwhelming majority (over 99) of the 96 of
  all species.

8
Distribution of Species in 18 Extant Clades w/
Convergent Image-Forming Eyes
Clade Species Number
Arthropods 839,000
Vertebrates 48,800
Cephalopods 650
Pectinacean Bivalves 410
Prionodontan Bivalves 216
Pontellid Copepods 140
Cypridinid Ostracods 105
Strombid Gastropods 80
Corycaeid Copepods 55
Sapphirinid Copepods 37
Alciopid Polychaetes 31
Heteropod Gastropods 30
Br. Sabellid Polychaetes 27
Cubozoan Cnidarians 25
Eu. Sabellid Polychaetes 18
Laternulid Bivalves 15
Bi. Sabellid Polychaetes 3
Me. Sabellid Polychaetes 1
9
Diversity Comparison of Extant Image-Forming
Clades with their Non-Visual Sister
Groups adapted from De Queiroz (1999)
Image-Forming Clade Diversity (Species No.) Non-Visual Sister Clade Diversity (Species No.) More or Less Diverse
Arthropods 839,000 Eucoelomate Protostomes 71,000
Vertebrates 48,815 Cephalochordates 23
Cephalopods 650 Gastropods 40,000 -
Pectinacean Bivalves 410 Anomiacean Bivalves 25
Prionodontan Bivalves 216 Mytilacean Bivalves 175
Corycaeid Copepods 56 Tuccid Copepods 1
Sapphirinid Copepods 37 Sabelliphilid Copepods 107 -
Alciopid Polychaetes 31 Eteonine Polychaetes 141 -
Cubozoan Cnidarians 17 Scyphozoan Cnidarians 200 -
Laternulid Bivalves 15 Periplomatid Bivalves 28 -
Megalomma Polychaetes 1 Demonax Polychaetes 8 -
10
Is Vision a Key Innovation?

• Above Data Suggests
• Neither image-forming eyes in general nor in
  particular contexts (active lifestyles) correlate
  strongly with differential patterns of diversity.
  
• On their face, these results appear to suggest
  that while image-forming eyes confer local
  adaptive benefits given the surprising number of
  independent (polyphyletic) origins, such
  increases in fitness do not seem to translate
  into adaptive radiations.
• But
• only measured net speciation
• Because neontological, addresses only long-term
  patterns of diversification not spatio-temporally
  localized macroevolutionary effects.
• visual acuity (minimum resolvable angle) (but see
  arthropods)

11
Paleontological Comparison of the Diversity of
Visual Clades for first 88 (my) adapted from
data drawn by de Queiroz, (2002) and Benton (1993)
Clade by Order of Appearance Mean No. Families for first 88 my
Fossil
Arthropods 73
Vertebrates 16
Cephalopods 31
Pectinacean Bivalves 2
Prionodontan Bivalves 3
Laternulid Bivalves 2
Heteropod Gastropods 4
Strombid Gastropods 2
Extant
Cubozoan Cnidarians 4
Pontellid Copepods 2
Corycaeid Copepods 2
Sapphirinid Copepods 2
Alciopid Polychaetes 2
Littorinid Gastropods 2
Br. Polychaetes 2
Eu. Polychaetes 2
Bi. Sabellid Polychaetes 2
Megalomma Polychaetes 2
12
Incumbent Advantage Hypothesis

• Two major gaps (i.e. major radiations) in the
  distribution of the mean numbers of families
• (1) Between the arthropods and all other groups,
  and
• (2) Between the arthropods, vertebrates and
  cephalopods and all other visual clades.
• This supports the Incumbent Advantage Hypothesis
• The early acquisition of a key innovation and its
  subsequent radiation may competitively dampen (or
  exclude) any future diversification in connection
  with the novel acquisitions of the trait
• Especially plausible in vision
• Once initial active predation evolved, remaining
  clades resorted to more inert or torpid modes of
  predator evasion (e.g. bivalves, echinoderms etc.

13
Vision and the Cambrian Explosion

• Explosive increase in diversity and disparity
  (morphospace occupation) (Foote Gould, 1992)
• Somewhat controversial (see Briggs et al. 1992)
• Trace Fossils Show Rapid Burst in Ecological /
  Functional Complexity (Conway Morris,
  1998a/1998b).
• Uncontroversial
• 1st Eye Appears in Trilobitidae 544 mya/
  C.E.
• Introduction of Vision-Supported
• Active Predation (Parker, 2004)
• Garden of Ediacara ? Arms Race
• (McMenamin McMenamin, 1990)
• Result (1) Advanced eyes in 2 other
• major clades, (2) hard-parts, (3) complex
• ecological strategies
• Right Eyed Arthropods and
• soon-to-be-eyed Vertebrates (Pikaia)

14
What Do I Mean By Robust Image Formation?

• Robust Image is one which represents the
  detailed, three-dimensional topography of an
  organisms surrounding environment, including the
  spatial arrangement of objects and object
  features, shapes, textures, depths and distances.
  
• Physical Image of an object or stimulus is a
  functional category that applies to the
  distribution of a stimulus on a sensory receptor
  surface
• The stimulus ultimately projected onto the
  senso-receptor array may be chemical (as in
  olfaction) or energetic (as in vision,
  echolocation, and electrogeneration).
• However, only energetic stimuli provide enough
  information about the environment for an organism
  to form what I call a robust image
• Moreover, apart from vision (which is passive)
  only active energetic image-formation (pulse
  emission) is adequate for the task

15
Echolocation

• Echoic Capabilities have evolved independently at
  least 5 times in the history of life, including 3
  orders of mammalsChiroptera (bats), Cetaceans
  (toothed whales), Insectivora (tree shrews)and
  two orders of birds Apodiformes (swiftlets) and
  Caprimulgiformes (oilbirds)
• Chiropterans form Robust Acoustic Images of their
  environment
• including the shapes, distances, textures, and
  spatial orientation of objects.
• can distinguish targets separated by distances
  well under 1mm in three dimensional space.
• Bats have a fine range resolution and are able to
  discriminate range differences on the order of 1
  cm at distances up to 240 cm

16
Chiropteran Echolocation as a Key Innovation

• One of the most diverse and ubiquitous orders of
  mammalsnearly 1/4 mammals is a bat.
• Also Sheer Biomass!
• Sister Taxa Comparison
• Bats gt1000 species vs. Dermoptera (4) or Tree
  Shrews (20)
• Microchiroptera (sophisticated echo) Vastly More
  Successful than Megachiroptera (reduced echo)
• Bats found on nearly every landmass except the
  polar regions and a few tropical islands
• Few natural (no specializing) predators
• except for R. Brandon
• Radiation at K-T boundary and suddenly appear
  over the entire globe completely developed (like
  eyes!) (Darwin)

17
Ecological Contingencies in Chiropteran
Echolocation

• Primary Bat Niche Aerial Insect Hawking
• Why did it take sophisticated echolocation take
  so long to evolve?
• Contingent on increases in aerial nocturnal
  pollinating insect densities (Lepidoptera and
  Diptera) due to angiosperm proliferation in the
  Cretaceous.
• Even so, why did bats develop echo first, before
  avians?
• Best Answer No aerial insectivorous birds or
  pterosaurs

18
Phylogenetic Contingencies in Chiropteran
Echolocation

• Active Biosonar / Robust Acoustic Image Formation
  requires high frequency signal emission
  capabilities
• This comes at a huge metabolic cost
• May be limited to Endothermic Vertebrates with
  directional sound capabilities (lungs / pharynx)
• Bats have reduced cost with the biomechanical
  coupling of echolocation and powered flight.
• Echo-then-Flight, Flight-First, Tandem Theories

19
Phylogenetic Contingencies in Chiropteran
Echolocation

• Order of Origin Bat Incumbent Advantage may have
  excluded Avian Echolocation (c.f. early eyes)
• I propose that sophisticated flying,
  echolocating, and nocturnally aerial hawking
  insectivorous bats expanded rapidly to fill much
  of this niche, preventing its occupation by
  subsequent avian clades who might hit upon the
  same Good Trick (echolocation).
• To use Darwins (1859) metaphor, bats have formed
  a wedge that is jammed so tightly in the economy
  of nature that no animal has subsequently been
  able to pry it out.
• Rudimentary Echolocation has evolved in
  Australasian swiftlets (edible nests) and the
  Neotropical oilbird (1 species).
• Do Not use echo to detect / capture prey
• Do Not form Robust Acoustic Images.
• No substantial macroevolutionary effects

20
Cetacean Echolocation

• Water represents another medium amendable to
  acoustic signaling, and thus it is the only other
  meta-habitat in which sophisticated active
  biosonar has evolved.
• Acoustic Image acuity / Robustness of dolphins is
  as good / better than bats
• Use Echolocation not only for object detection
  but also for small, medium, and large-scale
  navigation by locking onto landmarks.
• Use Echolocation not only for object detection
  but also for small, medium, and large-scale
  navigation by locking onto landmarks (unless
  pelagic).
• Holistic Representation of Objects
• Nearly 100 cross-modal recognitionEcho-to
  Vision and Vision-to Echo
• Echolocation is functionally equivalent to vision.

21
Contingency of Cetacean Echolocation

• Sister Taxa Comparison
• Odontoceti is a diverse sub-order, containing 10
  families and over 80 species, Mysticeti (baleen
  whales) are comprised of 4 families and only 14
  species.
• Complex echolocation, to the extent that it
  facilitates prey capture, navigation, and social
  communication may have played a key adaptive role
  in their relative success.
• Key Question If echolocation is such a Good
  Trick, Why has it not evolved in other closely
  related marine mammal taxa, or in any other taxa,
  for that matter?
• Do I hear the ring of contingency? Not
  necessarily
• Mysticeti or Sirenians?
• Why not Pinnipeds w/ similar foraging? (review
  shows they dont echo)
• Answer Due to their obligatory amphibious
  lifestyle (mating, etc.), retained the ability to
  hear on land /ice (i.e. in air, which has a
  different impedance than H20).
• Their ears are not adapted for exceptional
  full-time aquatic life necessary for robust
  echolocation
• Only endothermic fully aquatic fish-foraging
  animal is the cetacean!
• What about Fully Marine Reptiles, like
  Icythyosaur or Mosasaur? (ectothermic)

22
Robust Electrical Image Formation
schnauzenorgan
Mormyridae

• Electric Organ Discharges Independently Evolved
  in 2 grps of Weakly Electric Fish
• Electric Fovea
• The mormyrids have two specialized electric
  foveaeone in the nasal region for long-range
  guidance and object detection, and the other in
  schnauzenorgan, a long and flexible chin appendix
  covered with densely packed mormyromast
  electroreceptive cells, associated with
  shorter-range prey detection and discrimination.
• Like dual fovea in some birds (predator detection
  /flight and myopic foraging on ground)
• Objects can alter the electric organ discharge
  either in waveform or in amplitude, and the fish
  perceive both in order to assess object
  properties in multiple dimensions, including the
  objects the objects size, shape, spatial
  orientation, depth and distance, and complex
  impedance (passive and resistive components, and
  capacitance).
• Distance measure (via maximal slope) is
  unequivocal (unlike vision ambiguity), from which
  size can be positively derived
• Color Perception The detection of capacitance
  properties through (e.g.) waveform distortion can
  be compared to color vision which measures the
  wavelength of light reflected by an object.
• Holistic object perception trained to receive a
  positive reward (conspecific EOD) by learning and
  remembering to choose a metal cube (cylinder,
  pyramid, elliptical, etc.), they later preferred
  a plastic cube to a metal cylinder
• Alien Aspects of Electrolocation

Gymnotiformes
23
Electrolocation as a Key Innovation

• Sister Taxa Comparison
• Mormyridae is comprised of over 200 species, and
  is by far the largest family in its order, as the
  othersArapaimidae, Gymnarchidae, Hiodontidae,
  Notopteridae, Osteoglossidae, and
  Pantodontidaeall range from 1-5 species
• Advantages of Electrolocation
• EOD as behavioral isolating mechanisms
• Gymnotidae, while also successful (comprised of 5
  families, and nearly 200 species), are not nearly
  as diverse as their highly successful sister
  order Siluriformes (catfish), which contains 37
  families nearly 2,000 species, as well as a much
  wider geographical distribution.
• Nevertheless, electrogeneration is connected to
  substantial absolute diversification in both of
  the major taxa in which it has evolved.
• However, biogeographical ranges are
  circumscribed, perhaps due to limited ecological
  applicability.

24
Robust Image Formation and Complex Social Behavior

• Echolocation Sociality in Cetaceans
• Super-alliances (gt400), the largest known stable
  associations outside of humans.
• Social transmission of tool use
• Electrolocation Sociality in Fish
• Rather than converging on a single location for
  hunting, large predatory mormyrids of Lake Malawi
  (Africa) form cohesive traveling packs that
  forage as a unit through the cluttered rocky
  bottom for small cichlid prey.
• Form temporally stable associations gt 1 month
  that characterize pack hunting carnivores and
  cetaceans (Arnegard Carlson, 2005).
• EOD Synchronization
• Individual recognition

Pack-Hunting Mormyrids (Lake Malawi, Africa)
25
Other Macroevolutionary Effects of Robust Image
Formation

• Encephalization Related to Robust Image Formation
• Most Sophisticated Robust Image Forming Clades
  are More Encephalized than their sister taxa
• (1) Vision-Related Encephalization
• Vertebrates gt Echinoids
• Cephalopods gt Bivalves
• (2) Echolocation-Related Encephalization
• Dolphins gt Mysticeti
• Metacognition (delphinids)
• Bats gt Flying Lemurs or Tree Shrews
• (2) Electrolocation-Related Encephalization
• Mormyrids gt non-electric sister families
• Hypertrophied Mormyrocerebellum (at huge
  metabolic cost)
• Gymnotiformes gt Siluriformes