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Morphospace expansion paces taxonomic diversification after end Cretaceous mass extinction

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Highly resolved palaeontological records can address a key question about our current climate crisis: how long will it be before the biosphere rebounds from our actions? There are many ways to conceptualize the recovery of the biosphere; here, we focus on the global recovery of species diversity. Mass extinction may be expected to be followed by rapid speciation, but the fossil record contains many instances where speciation is delayed—a phenomenon about which we have a poor understanding. A probable explanation for this delay is that extinctions eliminate morphospace as they curtail diversity, and the delay in diversification is a result of the time needed for new innovations to rebuild morphospace, which can then be filled out by new species. Here, we test this morphospace reconstruction hypothesis using the morphological complexity of planktic foraminifer tests after the Cretaceous–Palaeogene mass extinction. We show that increases in complexity precede changes in diversity, indicating that plankton are colonizing new morphospace, then slowly filling it in. Preliminary diversification is associated with a rapid increase in the complexity of groups refilling relict Cretaceous ecospace. Subsequent jumps in complexity are driven by evolutionary innovations (development of spines and photosymbionts), which open new niche space. The recovery of diversity is paced by the construction of new morphospace, implying a fundamental speed limit on diversification after an extinction event.
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Articles
https://doi.org/10.1038/s41559-019-0835-0
1University of Texas Institute for Geophysics, Austin, TX, USA. 2Sam Houston State University, Huntsville, TX, USA. 3Present address: School of Earth
Sciences, University of Bristol, Bristol, UK. *e-mail: cmlowery@utexas.edu
Although present rates of extinction do not (yet1) rival the
‘big five’ mass extinctions, humanity is undeniably causing
elevated rates of biodiversity loss through climate change,
habitat destruction, invasive species introduction, and so on1. As we
seek to mitigate this loss, we must also learn how long it will take for
biodiversity and ecosystem functionality to recover after negative
anthropogenic effects subside. The Cretaceous–Palaeogene (K–Pg)
mass extinction, caused by the impact of an asteroid on the Yucatán
Platform in the southern Gulf of Mexico2, was the most recent and
most rapid of the five major mass extinctions and is perhaps the
only major event in Earth history that happened faster than mod-
ern climate change. Thus, it provides a unique analogue for future
recovery from rapid extinction.
Following the geologically instantaneous disappearance of a
huge portion of the biosphere, it may be presumed that survivors
would rapidly diversify to fill empty ecospace. The global recovery
of planktic foraminiferal diversity following the K–Pg mass extinc-
tion is a classic example of such explosive adaptive radiation37.
Survivor species, adapted for shallow water and marginal marine
environments, gave rise to dozens of new taxa that recolonized the
open marine ecospace vacated by the extinction event4,5,812. This
explosive radiation occurred in several pulses, the latter of which
were delayed for millions of years3,13,14. The initial early Danian burst
in diversity only added about 20 species—less than one-quarter of
pre-extinction diversity11. Global richness increased unsteadily
throughout the Palaeocene, and did not begin to approach even
mid-Cretaceous levels until the Palaeocene–Eocene boundary
10 Myr later (Fig. 1a). The full recovery of species or genus diversity
took more than 20 Myr, into the Middle Eocene15, at which point it
nearly matched the soaring heights of the Late Cretaceous.
Genus-level macrofaunal diversity data show that a 10-Myr delay
in elevated rates of origination is a feature of all mass extinctions,
including the K–Pg1618. This delay has also been identified in
marine plankton after the K–Pg (Fig. 1a)15,19,20, although its cause
remains unknown. Explanations have tended towards external
environmental controls, such as the delayed recovery of marine
export production4 or the persistence of toxic metals or other lin-
gering stressors affecting conditions in the upper water column
well after the extinction21, possibly driven by Deccan volcanism2225.
However, productivity was highly variable in the Early Palaeocene,
with some localities showing a geologically immediate increase after
the extinction26. Even considering the longest possible delay in the
recovery of global export productivity and the recolonization of
deeper habitats13,14 (about 4 Myr), this still does not provide a satis-
fying explanation for why diversity might remain low for so much
longer (up to 20 Myr). No evidence of toxic metal enrichments has
been found in Early Palaeocene sediments, and recent work within
the Chicxulub Crater, where impact-driven environmental contam-
ination would be worst, documented a rapid recovery there12. The
lack of a discernable environmental driver has led many authors to
propose that ecology, rather than environment, controls diversifica-
tion after a mass extinction12,26,27.
An important ecological control on diversification could be
the time needed to reconstruct morphospace within ecosystems17,
which we term the morphospace reconstruction hypothesis. We
often conceive of post-extinction radiations refilling empty niche
space, but as Kirchner and Weil17 pointed out, the reduction of
diversity caused by mass extinctions also destroys niche space (see
also Erwin’s excellent review28). Although ecological niches can be
conceptualized as slots in an ecosystem that different organisms
can fit into, they are actually created by, and are thus inseparable
from, the organisms that occupy them. In other words, organisms
themselves construct the environments they inhabit28. This can be
more properly conceived of as morphospace (that is, the range of
Morphospace expansion paces taxonomic
diversification after end Cretaceous mass
extinction
ChristopherM.Lowery 1* and AndrewJ.Fraass 2,3
Highly resolved palaeontological records can address a key question about our current climate crisis: how long will it be before
the biosphere rebounds from our actions? There are many ways to conceptualize the recovery of the biosphere; here, we focus
on the global recovery of species diversity. Mass extinction may be expected to be followed by rapid speciation, but the fossil
record contains many instances where speciation is delayed—a phenomenon about which we have a poor understanding. A
probable explanation for this delay is that extinctions eliminate morphospace as they curtail diversity, and the delay in diversi-
fication is a result of the time needed for new innovations to rebuild morphospace, which can then be filled out by new species.
Here, we test this morphospace reconstruction hypothesis using the morphological complexity of planktic foraminifer tests
after the Cretaceous–Palaeogene mass extinction. We show that increases in complexity precede changes in diversity, indicat-
ing that plankton are colonizing new morphospace, then slowly filling it in. Preliminary diversification is associated with a rapid
increase in the complexity of groups refilling relict Cretaceous ecospace. Subsequent jumps in complexity are driven by evo-
lutionary innovations (development of spines and photosymbionts), which open new niche space. The recovery of diversity is
paced by the construction of new morphospace, implying a fundamental speed limit on diversification after an extinction event.
NATURE ECOLOGY & EVOLUTION | VOL 3 | JUNE 2019 | 900–904 | www.nature.com/natecolevol
900
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... Fortunately, two important autotrophic and heterotrophic components have excellent fossil records i.e. calcareous nannoplankton (haptophyte algae) and planktic foraminifera (shellbuilding micro-zooplankton) that provide representative signals of the pelagic ecosystem. Differences in rates of recovery of the biological pump, plankton diversity and size are apparent in the fossil record [30,31,[34][35][36][37]. Recently, post-K/Pg ecosystem recovery, assessed via community stability history of nannofossils, has been linked to a return of the biological pump in the Pacific, approximately 1.8 Myr years after the event [31]. ...
... Environmental conditions feedback on the diversity and abundance of marine organisms [48][49][50] and thereby change the fixation and export of carbon and utilization of nutrients. As marine ecospace was re-created [28,36,51], rates of evolutionary turnover were far above typical background rates [34]. Small, opportunistic planktic foraminifera dominate the early Danian [29] and a high frequency of morphological abnormalities in Tunisian planktic foraminifera has been linked to severe environmental instability [52]. ...
... Concurrently, the recovery of the biological pump does not result in a recovery of diversity and pre-extinction organism size [31]. The process of biotic recovery may be governed by other factors, such as niche creation, which are suggested to work on much longer time scales [36,67]. This interpretation supports the notion that rather than there being predefined 'niche' space (i.e. ...
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The ocean biological pump is the mechanism by which carbon and nutrients are transported to depth. As such, the biological pump is critical in the partitioning of carbon dioxide between the ocean and atmosphere, and the rate at which that carbon can be sequestered through burial in marine sediments. How the structure and function of planktic ecosystems in the ocean govern the strength and efficiency of the biological pump and its resilience to disruption are poorly understood. The aftermath of the impact at the Cretaceous/Palaeogene (K/Pg) boundary provides an ideal opportunity to address these questions as both the biological pump and marine plankton size and diversity were fundamentally disrupted. The excellent fossil record of planktic foraminifera as indicators of pelagic-biotic recovery combined with carbon isotope records tracing biological pump behaviour, show that the recovery of ecological traits (diversity, size and photosymbiosis) occurred much later (approx. 4.3 Ma) than biological pump recovery (approx. 1.8 Ma). We interpret this decoupling of diversity and the biological pump as an indication that ecosystem function had sufficiently recovered to drive an effective biological pump, at least regionally in the South Atlantic.
... A state transition 2 → 1 corresponds to this scenario. The life recovery rate was included in the model only as a comparison to findings from macrofaunal diversity data, which show that all mass extinctions have a 10-Myr 'speed rate' in diversity recovery (Alroy, 2008;Lowery and Fraass, 2019). However, unlike diversity, morphological complexity can be rebounded more quickly, reaching a plateau within ∼ 5 Myr following the Cretaceous mass extinction, as shown for planktic foraminifera (Lowery and Fraass, 2019). ...
... The life recovery rate was included in the model only as a comparison to findings from macrofaunal diversity data, which show that all mass extinctions have a 10-Myr 'speed rate' in diversity recovery (Alroy, 2008;Lowery and Fraass, 2019). However, unlike diversity, morphological complexity can be rebounded more quickly, reaching a plateau within ∼ 5 Myr following the Cretaceous mass extinction, as shown for planktic foraminifera (Lowery and Fraass, 2019). Furthermore, we let a life-terminated host become habitable again at a rate of τ R = 0.2, i.e., state transition 2 → 0. ...
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... Gastropod species richness took approximately 7-8 Myr to recover (Fig. 1). Translating this to the current biodiversity crisis suggests that even if anthropogenic impact on the world's biota ceases immediately, the already triggered phase of extinction might still involve several million years and so will faunal recovery 50,51 . Given the extremely fast pace at which global change happens today and the high rates of extinction predicted for the next decades, both of which outpace the rates for the 5 th mass extinction, Europe's freshwater biota may face an even more dramatic collapse in the near future than after the asteroid impact 66 Myr ago. ...
... Similarly, many Mesozoic species lack sufficient diagnostic features that allow clear assignment to a specific family. It has also been shown that the use of genus-level data can severely bias the outcomes of evolutionary studies 59 , many of which currently focus on the specieslevel data 35,50,51,54 . ...
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... Kirchner & Weil (2000) speculated that this was driven by the need to rebuild ecospace following mass extinctions, as life strategies disappear along with species during such events. Lowery & Fraass (2019) tested this hypothesis with the record of planktic foraminifer morphological complexity (essentially ecospace occupation in simple groups such as foraminifera) following the K-Pg mass extinction and found that ecospace expansion does indeed pace diversification. This suggests a fundamental macroevolutionary speed limit on diversification after mass extinctions. ...
... The appearance of incoming species of planktic foraminifera and nannofossils characteristic of deeper water depth habitats suggests a first step for the recolonization of deeper niches. However, it is well-known that the entire reoccupation of the deeper ocean niches by planktic foraminifera, as well as the rebound of diversity levels comparable to pre-KBP levels, took several million years (Aze et al., 2011;Birch et al., 2012Birch et al., , 2016Lowery and Fraass, 2019). Within PFAS-3α, carbonate parameters (%CaCO 3 and the fragmentation index) are similar to those in PFAS-2. ...
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... Kirchner & Weil (2000) speculated that this was driven by the need to rebuild ecospace following mass extinctions, as life strategies disappear along with species during such events. Lowery & Fraass (2019) tested this hypothesis with the record of planktic foraminifer morphological complexity (essentially ecospace occupation in simple groups such as foraminifera) following the K-Pg mass extinction and found that ecospace expansion does indeed pace diversification. This suggests a fundamental macroevolutionary speed limit on diversification after mass extinctions. ...
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The paper documents evolutionary patterns of morphological disparity in Ordovician-Devonian crinoids, using a set of 75 discrete characters covering the principal features of the crinoid stem, cup, tegmen, and arms. Discrepancy is measured as the average dissimilarity among species, the range of morphospace occupied, and the number of realized character-state combinations. Comparison with generic richness reveals that the full range of form was essentially attained by the early part of the Caradocian, long before the time of maximal taxonomic diversity. Despite subsequent taxonomic diversification, the variety of crinoid form did not expand appreciably; increased diversity was accommodated by the evolution of variations upon the spectrum of designs established earlier. -from Author
Article
The earliest Paleocene record of calcareous nannoplankton presents a unique opportunity to understand the evolutionary recovery of life from mass extinction. Nannoplankton were devastated at the Cretaceous/Paleogene boundary and their subsequent recovery can be studied in great detail because of their abundance in sediments, continuous stratigraphic occurrence, and near global distribution. Here we determine when and where new species of nannoplankton originated and how they dispersed following the Cretaceous/Paleogene mass extinction. Initially, we focus our efforts on North Pacific and South Atlantic deep sea sites with orbital age control to compare the precise timing and dynamics of the recovery between the locations. We then broaden our investigation to six sites from different basins and a variety of environments to study global patterns of the initial recovery. Our results show that many taxa in key Paleogene lineages originated in the North Pacific Ocean and that assemblages comprised primarily of new Paleogene taxa were not observed at other sites for several hundred thousand years. Survivors that were adapted to eutrophic post extinction conditions rapidly expanded in Southern Hemisphere sites where they dominated assemblages for most of the initial recovery. We therefore hypothesize that groups of survivors formed regionally incumbent assemblages in the Southern Hemisphere that limited diversification and dispersal of new Paleogene taxa. The end of survivor dominance correlates to the recovery of the biologic pump and subsequent decrease in surface ocean nutrient concentration 300–400 Kyr after the boundary. Only after survivors were removed did new Paleogene nannoplankton assemblages become abundant globally. Our results indicate that competition from regionally incumbent survivors was as an important control on the K/Pg recovery of nannoplankton.