Whether equilibrium dynamics between extinction and processes generating new species governs biodiversity, or instead stochastic changes shape diversity over time is one of the central questions in evolutionary biology. But tests of equilibrium dynamics since MacArthur and Wilson formulated their model have primarily involved colonization and extinction, neglecting speciation. Analyses using recently developed algorithms fitted to branching times for both extant and extinct bats from the Greater Antilles reveal a 20-40-million year equilibrium between high extinction rates offset by both colonization and speciation. Since at least 13 species have gone extinct over the last 20,000 years, however, this fauna is no longer in equilibrium. It would take millions of years for dynamics were to restore the lost diversity to their equilibrium preceding the Holocene. There is a longstanding debate on whether this pulse of mammalian extinction, which extended to all of North America, is linked to human colonization, or instead corresponds to the loss of island area and climate change at the end of the last glaciation. On the islands, however, humans only arrived a few thousand years ago, providing an opportunity to test these hypotheses. Bayesian models of the difference between faunal last appearance and human first appearance, together with the largest database of archaeological and paleontological radiocarbon dates reveal the majority of extinction events occurred after human arrival. While some large bodied species were lost soon after human colonization and may have been hunted, others may have been vulnerable to pre-Columbian agriculture, and many more to predators introduced during European colonization. The demise of the Caribbean mammal fauna as a result of increasing human transformation of local ecosystems provides lessons for our own time and the extinction events today and into the future.

1. Twenty million years of extinction and
survival in the Caribbean
Liliana M. Dávalos
Ecology, Evolution, and Behavior Seminar
University of Minnesota

2. What we do in the lab
The Dávalos Lab

3. A double mission
Biological
diversity
Evolution Extinctionincrease decrease

4. MacArthur & Wilson 1963 Evolution

5. Equilibrium dynamics
• Scaling of richness
• Stability
• Predictable

6. Disequilibrium
dynamics
• Under-scaling of richness
• Instability
• Unpredictable

7. Most tests = dynamics
from scaling
Morgan & Woods 1986 Biol. J.
Linnean Soc.
Scaling
Scaling (ancient)

8. Evolutionary dynamics Ricklefs & Bermingham 2001 Science
Scaling

9. Only two elements Ricklefs & Bermingham 2001 Science
Extinction
Colonization

10. (Some) Bats of the Caribbean
Rojas, Warsi, Dávalos 2016 Syst. Biol.
Tavares, Warsi, … Dávalos 2018 J. Biogeogr.

11. Data on Greater
Antillean bats
Valente, Etienne, Dávalos 2017 Nature Ecol. & Evol.

12. Equilibrium, three
elements
Time before present (106 years)
Valente, Etienne, Dávalos 2017 Nature Ecol. & Evol.
Which
scaling?

13. Equilibrium dynamics!
Time before present (106 years)
Valente, Etienne, Dávalos 2017 Nature Ecol. & Evol.
Age λc μ γ λa
20 0.22 0.26 0.017 0.27
45 0.26 0.35 0.021 0.27

14. What about extinct
species?
Valente, Etienne, Dávalos 2017 Nature Ecol. & Evol.

15. Fossils make a
difference
Age
Ma
λc μ γ λa
20 0.28 0.33 0.030 0.19
45 0.32 0.41 0.036 0.16
Age
Ma
λc μ γ λa
20 0.22 0.26 0.017 0.27
45 0.26 0.35 0.021 0.27
Valente, Etienne, Dávalos 2017 Nature Ecol. & Evol.

16. 0 10 20 30 40
020406080
Numberofendemicspecies
01020304050
Numberofendemicspecies
Time (Ma)
Restoring richness takes
time
Valente, Etienne, Dávalos 2017 Nature Ecol. & Evol.

17. Highlights 20 Ma
• Equilibrium upended by
recent extinctions
• Fossils change rates of
colonization, not just
extinction
• Scaling, stable,
predictable
• Time to recovery long
Photo by Jon Flanders

19. What killed the mammals
of the Caribbean?
Deglaciation!
© Adrian Tejedor

20. Islands of the Caribbean:
The West Indies
Dávalos,& Turvey 2012 Bones, Clones, and Biomes

21. Dávalos & Russell 2012 Ecol. Evol.

22. But there were no dates Soto-Centeno & Steadman 2015 Sci. Rep.

23. Timing is everything Cooke, Dávalos et al. 2017 Annu. Rev. Ecol. Evol. Syst.

25. A hierarchical model
• Difference in dates
• Clustered by island
• Can be affected by
the type of dating or
remains
• Positive = after
humans

26. Large islands: Two
extinction waves
• Larger islands, some
pre-human extinctions
• Not all extinction
caused by humans
• Another cluster of
extinction after human
arrival
• Humans likely
responsible for
some losses
Cooke, Dávalos et al. 2017 Annu. Rev.
Ecol. Evol. Syst.

27. Lesser Antilles: One
extinction wave
• Many smaller
mammals survived
human use
• Found in middens,
presumably eaten
• But could not recover
after European arrival
• Cats, rats, mice,
goats, introduced

28. Lessons from Marie
Galante
Stoetzel et al. 2016 Quat. Sci. Rev.

29. Many species lack
dates
• Some islands/clades
well studied
• Many missing
• Rodents & bats
• Even in Greater
Antilles
• Too few dates
• But we know one
thing…
Cooke, Dávalos et al. 2017 Annu. Rev.
Ecol. Evol. Syst.

30. Phylogeny!
• Some Caribbean
groups distinct
• e.g., Solenodon
• Others less distinct
• Some hutias &
Short-faced bats
• Not enough life history
Cooke, Dávalos et al. 2017 Annu. Rev.
Ecol. Evol. Syst.

31. A few traits
• Bat extinction
• Larger species
• Herbivores
• Non-bats
• Larger
• Smaller?!
Cooke, Dávalos et al. 2017 Annu. Rev.
Ecol. Evol. Syst.

32. Mammals of the Caribbean today
© Yomangani/Creative Commons © Eladio Fernandez
© Jon Flanders

33. Survivors are on the
brink of extinction
• Among bats
• 9 of 60 threatened
• 3 known from 1
cave each
• Among non-bats
• 8 of 12 threatened
• How to predict
extinction or
survival?
Illustration by Adrián Tejedor
Cooke, Dávalos et al. 2017 Annu. Rev.
Ecol. Evol. Syst.

34. Modeling extinction/
survival
In progress

35. Modeling extinction/
survival
In progress
Spp. traits
Island characteristics
Mass is quadratic
Many island characteristics
can be added

36. Intercept on probability of survival
−2000 −1000 0 1000 2000
Standard deviation
Mean
Zygodontomys_sp
Xenothrix_mcgregori
Xaymaca_fulvopulvis
Tainotherium_valei
Solenodon_paradoxus
Solenodon_marcanoi
Solenodon_cubanus
Solenodon_arredondoi
Sheep_Pen_femur_unidentified_rodent_taxon
Rhizoplagiodontia_lemkei
Quemisia_gravis
Plagiodontia_velozi
Plagiodontia_spelaeum
Plagiodontia_aedium
Pennatomys_nivalis
Parocnus_serus
Parocnus_browni
Paralouatta_varonai
Oryzomys_antillarum
Oryzomyini_undescribed_species_small_Montserrat_taxon
Oryzomyini_undescribed_species_small_Grenada_taxon
Oryzomyini_undescribed_species_large_Montserrat_taxon
Oryzomyini_undescribed_species_large_Grenada_taxon
Oryzomyini_undescribed_species_St._Martin_taxon
Oryzomyini_undescribed_species_Saba_taxon
Oryzomyini_undescribed_species_Anguilla_taxon
Oligoryzomys_victus
Nesophontes_zamicrus
Nesophontes_sp2
Nesophontes_sp1
Nesophontes_paramicrus
Nesophontes_micrus
Nesophontes_hypomicrus
Nesophontes_edithae
Neocnus_toupiti
Neocnus_gliriformis
Neocnus_dousman
Neocnus_comes
Mysateles_prehensilis
Mesocapromys_sanfelipensis
Mesocapromys_nanus
Mesocapromys_melanurus
Mesocapromys_kraglievichi
Mesocapromys_auritus
Mesocapromys_angelcabrerai
Megalomys_luciae
Megalomys_georginae
Megalomys_desmarestii
Megalomys_audreyae
Megalocnus_zile
Megalocnus_rodens
Macrocapromys_latus
Macrocapromys_acevedo
Isolobodon_portoricensis
Isolobodon_montanus
Insulacebus_toussaintiana
Hyperplagiodontia_araeum
Hexolobodon_phenax
Heteropsomys_insulans
Geocapromys_thoracatus
Geocapromys_sp2
Geocapromys_sp1
Geocapromys_ingrahami
Geocapromys_columbianus
Geocapromys_brownii
Elasmodontomys_obliquus
Clidomys_osborni
Capromys_sp1
Capromys_pilorides
Brotomys_voratus
Brotomys_contractus
Boromys_torrei
Boromys_offella
Antillothrix_bernensis
Antillomys_rayi
Acratocnus_ye
Acratocnus_simorhynchus
Acratocnus_odontrigonus
Acratocnus_antillensis
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Initial results species
• Species vary in
probability of survival
• Some appear doomed

37. Initial results islands
• Multiple islands were/
became extinction
traps

38. Initial results
predictors
• Island area weakly
related to survival
• Elevation strong
predictor extinction
• Intuition about large
and small spp. correct!

39. A history of extinction Cooke, Dávalos et al. 2017 Annu. Rev. Ecol. Evol. Syst.

40. A history of people
• Humans arrived in four
waves
• First three waves
from New World
• Introduced dogs
and agriculture
• Last wave from Old
World
• Introduced
invasive spp.
©Theodor de Bry/National Library of Medicine

41. Larger mammals probably hunted early on
© Ghedoghedo Wilson 1989 J Field Archaeol.

42. Many extinction events recorded after arrival of Old World
invasive competitors/predators
Turvey et al. 2012 Mamm. Biol.

43. Agriculture likely important for certain species
© Adrian Tejedor ©Pierpont Morgan Library

44. Highlights
• Multiple causes of
extinction
• Some before humans
• Most after humans
• Small AND large
terrestrial species went
extinct
• not just hunting
• Agriculture maybe
important for bats, others
© Yomangani/Creative Commons

45. Why is this important? The world is made of islands

46. This is happening now Ray et al. 2015 Mongabay

47. What happens when the
frontier closes?
1869

48. Frontier closes, forest
vanishes
Stanton 2014 Biol. Cons.

49. The frontier
• Border between settled
land/ natural habitats
• Forest->property
• Final condition = no
forest
• Happened in other
regions
• Most of Andes hotspot
• Unfolding in most of
Amazonia Etter et al. 2006 J. Environ.
Manage.
Fractionforest

50. The Amazon frontier A general model
Fractionforest
beachhead
Time ->
mixed agriculture
properties
pastures!

51. The sixth extinction is
(partially) avoidable
• Equilibrium is real
• Habitat loss = extinction
• Fragmentation = extinction
• We have the tools to conserve
• Connect ecosystems
• ~30 years before Amazon
becomes pastures
• We are responsible for
evolution into the future

52. Thanks!