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Is Robust Image Formation a
Key Innovation?
Predictability and Contingency in
Macroevolution
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 adaptations—they must be key
adaptations, likely to evolve iteratively and to have substantial
macroevolutionary effects.
– Dennett (‘95), Dawkins (’04), and Conway Morris (0’3) 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?
What Do I Mean By ‘Robust’ Image Formation?
• Robust Image is one which represents the detailed, threedimensional topography of an organism’s 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
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)
Iterative Evolution of Camera-Type Eyes
• Camera-type eyes have evolved
independently in 5 phyla, including
molluska, chordata, annelida, cnidaria,
and arthropoda
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)
Image-Forming Eyes and Diversification:
An Empirical Investigation
Land and Fernald’s (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 phyla—namely,
Cnidaria, Molluska, Annelida, Arthropoda, and Chordata—account
for over 96% of the known species (Land & Fernald, 1992).
• Isn’t 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 eyes—namely the arthropods
and vertebrates—account for the overwhelming majority (over 99%) of
the 96% of all species.
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
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
Arthropods
839,000
Eucoelomate
Protostomes
Vertebrates
48,815
Cephalochordates
Diversity
(Species No.)
More or Less
Diverse
71,000
+
23
+
40,000
-
Cephalopods
650
Gastropods
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
-
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)
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
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.
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  Arm’s 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)
What Do I Mean By ‘Robust’ Image Formation?
• Robust Image is one which represents the detailed, threedimensional topography of an organism’s 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
Echolocation
• Echoic Capabilities have evolved independently at least
5 times in the history of life, including 3 orders of
mammals—Chiroptera (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
Chiropteran Echolocation as a Key Innovation
•
One of the most diverse and ubiquitous orders of mammals—nearly 1/4
mammals is a bat.
– Also Sheer Biomass!
•
•
Sister Taxa Comparison:
• Bats >1000 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)
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
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
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 Darwin’s (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
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 recognition—Echo-to Vision and Vision-to
Echo
– Echolocation is functionally equivalent to vision.
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 don’t 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)
schnauzenorgan
Robust Electrical Image Formation
Mormyridae
•
•
Electric Organ Discharges: Independently Evolved in 2 grps of Weakly Electric Fish
Electric Fovea:
–
–
•
The mormyrids have two specialized electric foveae—one 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 object’s the object’s 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
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 others—Arapaimidae,
Gymnarchidae, Hiodontidae, Notopteridae, Osteoglossidae, and
Pantodontidae—all 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.
Robust Image Formation and Complex Social Behavior
• Echolocation & Sociality in Cetaceans:
– Super-alliances (>400), 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 [> 1 month] that
characterize pack hunting carnivores and cetaceans”
(Arnegard & Carlson, 2005).
– EOD Synchronization
– Individual recognition
Pack-Hunting Mormyrids (Lake Malawi, Africa)
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 > Echinoids
Cephalopods > Bivalves
(2) Echolocation-Related Encephalization:
•
•
Dolphins > Mysticeti
• Metacognition (delphinids)
Bats > Flying Lemurs or Tree Shrews
(2) Electrolocation-Related Encephalization:
–
Mormyrids > non-electric sister families
»
–
Hypertrophied ‘Mormyrocerebellum’ (at huge metabolic cost)
Gymnotiformes > Siluriformes