Large-scale evolutionary trends

1. Large-scale evolutionary trends Foraminiferal size, oxygen and photosymbiosis

2. 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

3. Evolution of size Cope’s rule: Tendency in animal groups to evolve toward larger size First articulated in 1870s Size trends recognized in reptiles, mammals, arthropods, mollusks

4. 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. 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 absolute minimum size There’s always room at the top Increasing size

5. 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

6. ~ 3 cm

7. Foram sculpture park (China)

8. live foram assemblage

9. semelparous reproduction

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

11. arrowhead made of silicified fusulinid limestone fusulinid limestones

12. 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)

13. dramatic size evolution in fusulinids

14. “Passive” vs. “Driven” trends PASSIVE DRIVEN No confining boundary; increases more likely than decreases (implies selection for large size) Confining lower boundary; increases and decreases equally likely McShea 1994 Evolution

15. Minimum test PASSIVE DRIVEN Minimum does not increase Minimum increases McShea 1994 Evolution

16. Minimum test suggests adriven trend

17. 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

18. Fusulinid size distribution Volume (mm3)

19. Subclade test suggests a driven trend parent clade

20. 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 = SCbetweengroups + SCwithingroups + SCheteroskedacticity

21. indicates passive trend Each subclade exhibits a normal distribution, but subclade means are not normally distributed about the parent clade mean Wang 2001 Evolution

22. indicates driven trend Subclade means are normally distributed about the parent clade mean, but each subclade is right-skewed Wang 2001 Evolution

23. 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

24. Analysis of skewness(fusulinid dataset) Total skewness of fusulinoidean volume distribution as the sum of three components. Category Value % Trend indicated Skewness within subclades 204,892,468 67.01 driven Skewness between subclades -295,643 -0.10 passive Heteroskedasticity skewness 101,161,672 33.09 passive Total skewness 305,758,497 100.00

25. Interpretation of results Size trend in fusulinids is 2/3 driven and 1/3 passive Driven component likely reflects selection for large size Large size as a result of photosymbiosis Passive component likely reflects relaxed constraints on size Large size permitted by hyperoxia

26. 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 Symbionts include diatoms, dinoflagellates, unicellular green algae, unicellular red algae and cyanobacteria

27. Photosymbionts in live foram and coral National Geographic image courtesy of Pam Hallock

28. foram with photosymbionts image courtesy of Pam Hallock

29. Symbionts cultured from live foram 20 µm image courtesy of Scott Fay & Jere Lipps

30. Benefits of photosymbiosis Energy Mixotrophic nutrition (feeding & photosynthesis) Calcification ATP energy for concentrating inorganic carbon; removal of ions that inhibit calcification Removal of host metabolites by symbionts

31. Characteristics of modern, symbiont-bearing forams Preference for tropical, oligotrophic habitats Stable environment; protected from continental and seasonal influences Unique life history strategy Large size (delayed reproductive maturity) Production of few, large embryons with low mortality

32. Giant embryons? Fusulinid with spherical adult shell and elongate interior

33. Oxygen & size Surface Volume2/3 Availability of oxygen constrains maximum cell size 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 Radius = 2 Surface = 50.3 Volume = 33.5 × 2 Radius = 1 Surface = 12.6 Volume = 4.2 Four-fold increase in surface Eight-fold increase in volume

34. Late Paleozoic hyperoxia

35. Oxygen & size size increase associated with equally dramatic increase in atmospheric oxygen

36. Linear regression analysis p = 0.0002 r2 = 0.41

37. 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)