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 Tendency in animal groups to

evolve toward larger sizeo First articulated in 1870s o 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.

absoluteminimum

size

If extinction vacates organisms in a givensize class, others from adjacent size classes

might increase or decrease in size in order to fill the void There’salways room

at the top

Increasing size

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

semelparousreproduction

Fusulinid forams

• Originated ~330 Ma; became extinct ~250 Ma• Very abundant & diverse; “rock-building” protists• Many lineages achieved “gigantic” size

arrowhead made of silicifiedfusulinid 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 evolutionin fusulinids

McShea 1994 Evolution

Confining lower boundary;increases and decreases

equally likely

No confining boundary;increases more likely

than decreases (impliesselection for large size)

PASSIVE DRIVEN

“Passive” vs. “Driven” trends

McShea 1994 Evolution

PASSIVE DRIVEN

Minimum does not increase Minimum increases

Minimum test

Minimum test suggests adriven trend

McShea 1994 Evolution

Subclade test:Size distribution of parent clade is nearly always right-skewed.

Subclade from the tail of theparent clade’s distributionis right-skewed

Subclade from the tail of theparent clade’s distributionis not skewed

Fusulinid size distribution

Volume (mm3)

parent clade

Subclade test suggests a driven trend

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

Each subclade exhibits a normal distribution, butsubclade means are not normally distributed

about the parent clade mean

indicatespassive trend

Wang 2001 Evolution

Subclade means are normally distributedabout the parent clade mean, but each

subclade is right-skewed

indicatesdriven trend

Wang 2001 Evolution

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

indicatespassive trend

Wang 2001 Evolution

Analysis of skewness(fusulinid dataset)

100.00305,758,497Total skewness

passive33.09101,161,672Heteroskedasticity skewness

passive-0.10-295,643Skewness between subclades

driven67.01204,892,468Skewness within subclades

Trend indicated%ValueCategory

Total skewness of fusulinoidean volume distribution as the sum of three components.

Interpretation of results

• Size trend in fusulinids is 2/3 driven and 1/3 passive

• Driven component likely reflects selection for large sizeo Large size as a result of photosymbiosis

• Passive component likely reflects relaxed constraints on sizeo 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 familieso 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

image courtesy of Scott Fay & Jere Lipps

20 µm

Benefits of photosymbiosis

• Energyo 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 habitatso Stable environment; protected from continental and

seasonal influences• Unique life history strategy

o Large size (delayed reproductive maturity)o Production of few, large embryons with low mortality

Giant embryons?

Fusulinid withspherical adult shelland elongate interior

Oxygen & size

• Availability of oxygen constrains maximum cell size

Surface Volume2/3

As the linear dimensions of an object increase by a factor of X, itssurface area increases by X2 while its volume increases by X3

Radius = 1Surface = 12.6Volume = 4.2

Radius = 2Surface = 50.3Volume = 33.5

Four-fold increase in surfaceEight-fold increase in volume

× 2

Late Paleozoic hyperoxia

Oxygen & size

size increase associatedwith equally dramaticincrease in atmosphericoxygen

p = 0.0002r2 = 0.41

Linear regression analysis

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)