Large-scale
evolutionary trends
Foraminiferal size, oxygen and
photosymbiosis
Outline
• Cope’s rule
• What are foraminifera?
• Dramatic size increase in late Paleozoic
fusulinid foraminifera
• Passive and driven evolutionary trends
• Tests for analyzing the fusulinid size trend
• Interpretation of results
Evolution of size
• Cope’s rule:
o
o
o
Tendency in animal groups to
evolve toward larger size
First articulated in 1870s
Size trends recognized in reptiles,
mammals, arthropods, mollusks
Cope’s rule: Traditional explanation
• The largest size class is always unoccupied. Therefore,
over time the number of size classes will increase since the
one at the top is always open and available to be filled.
absolute
minimum
size
If extinction vacates organisms in a given
size class, others from adjacent size classes
might increase or decrease in size in order to fill the void
Increasing size
There’s
always room
at the top
What are foraminifera?
• Living protists with fossil record dating back to
Cambrian Period (500 myr)
• 5,000 living species; >100,000 fossil species
• Marine, brackish and freshwater
• Benthic and planktonic (20% of total modern
carbonate production)
• Most studied group of fossils
~ 3 cm
Foram sculpture park (China)
live foram assemblage
semelparous
reproduction
Fusulinid forams
• Originated ~330 Ma; became extinct ~250 Ma
• Very abundant & diverse; “rock-building” protists
• Many lineages achieved “gigantic” size
arrowhead made of silicified
fusulinid limestone
fusulinid limestones
Fusulinid forams
Large specimens can reach 16 mm in length and 8 mm in diameter
(volume = 500 mm3 surface area = 340 mm2)
Smallest specimen is 0.06 mm in length and 0.15 mm in diameter
(volume = 0.01 mm3 surface area = 0.04 mm2)
dramatic size evolution
in fusulinids
“Passive” vs. “Driven” trends
PASSIVE DRIVEN
Confining lower boundary;
increases and decreases
equally likely
No confining boundary;
increases more likely
than decreases (implies
selection for large size)
McShea 1994 Evolution
Minimum test
PASSIVE DRIVEN
Minimum does not increase
Minimum increases
McShea 1994 Evolution
Minimum test
suggests a
driven trend
Subclade test:
Size distribution of parent clade is nearly always right-skewed.
Subclade from the tail of the
parent clade’s distribution
is not skewed
Subclade from the tail of the
parent clade’s distribution
is right-skewed
McShea 1994 Evolution
Fusulinid size distribution
Volume (mm3)
Subclade test suggests a driven trend
parent clade
Quantifying passive and driven
components of large-scale trends
• Wang (2001) recognized that large-scale trends are unlikely to
be entirely passive or entirely driven, but rather a combination
of both types
• Analysis of skewness test determines the proportional
influence of passive and driven mechanisms: Sums of Cubes
SCtotal = SCbetween groups + SCwithin groups + SCheteroskedacticity
indicates
passive trend
Each subclade exhibits a normal distribution, but
subclade means are not normally distributed
about the parent clade mean
Wang 2001 Evolution
indicates
driven trend
Subclade means are normally distributed
about the parent clade mean, but each
subclade is right-skewed
Wang 2001 Evolution
indicates
passive trend
Subclade means are normally distributed about the parent clade mean,
and each subclade is normally distributed, but standard deviation is
greater for subclades near right tail of parent clade’s distribution
Wang 2001 Evolution
Analysis of skewness
(fusulinid dataset)
Total skewness of fusulinoidean volume distribution as the sum of three components.
Category
Value
%
Trend indicated
204,892,468
67.01
driven
-295,643
-0.10
passive
Heteroskedasticity skewness
101,161,672
33.09
passive
Total skewness
305,758,497
100.00
Skewness within subclades
Skewness between subclades
Interpretation of results
• Size trend in fusulinids is 2/3 driven and 1/3
passive
• Driven component likely reflects selection for
large size
o
Large size as a result of photosymbiosis
• Passive component likely reflects relaxed
constraints on size
o
Large size permitted by hyperoxia
Photosymbiosis in forams
• Early suggestions of photosymbiosis in living
forams (1880s — 1950s)
• Lee et al. (1965) established first unequivocal
evidence for photosymbiosis in living forams
• Photosymbionts now confirmed in 12 extant
families
o
Symbionts include diatoms, dinoflagellates, unicellular
green algae, unicellular red algae and cyanobacteria
Photosymbionts in live
foram and coral
National Geographic
image courtesy of Pam Hallock
foram with photosymbionts
image courtesy of Pam Hallock
Symbionts cultured from live foram
20 µm
image courtesy of Scott Fay & Jere Lipps
Benefits of photosymbiosis
• Energy
o
Mixotrophic nutrition (feeding &
photosynthesis)
• Calcification
o
ATP energy for concentrating inorganic carbon;
removal of ions that inhibit calcification
• Removal of host metabolites by symbionts
Characteristics of modern,
symbiont-bearing forams
• Preference for tropical, oligotrophic habitats
o
Stable environment; protected from continental and
seasonal influences
• Unique life history strategy
o
o
Large size (delayed reproductive maturity)
Production of few, large embryons with low mortality
Giant embryons?
Fusulinid with
spherical adult shell
and elongate interior
Oxygen & size
• Availability of oxygen constrains maximum
cell size
Surface
2/3
Volume
As the linear dimensions of an object increase by a factor of X, its
surface area increases by X2 while its volume increases by X3
×2
Radius = 1
Surface = 12.6
Volume = 4.2
Radius = 2
Surface = 50.3
Volume = 33.5
Four-fold increase in surface
Eight-fold increase in volume
Late Paleozoic hyperoxia
Oxygen & size
size increase associated
with equally dramatic
increase in atmospheric
oxygen
Linear regression analysis
p = 0.0002
r2 = 0.41
Conclusions
• Fusulinid size evolution was
mostly a driven response to
photosymbiosis (selection for large
size)
• BUT, a significant part of the trend
was passive size increase in
response to increasing oxygen
availability (increase in the upper
bound to cell size)