A phylogeny of Cenozoic macroperforate planktonic foraminifera from fossil data

Aze, Tracy; Ezard, Thomas H. G.; Purvis, Andy; Coxall, Helen K.; Stewart, Duncan R. M.; Wade, Bridget S.; Pearson, Paul Nicholas

doi:10.1111/j.1469-185x.2011.00178.x

Cited by 222 publications

(423 citation statements)

References 126 publications

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“…We do so by analyzing the recently published phylogeny of Aze et al (24), using a unique approach that incorporates assumptions i-iii above while taking into account uncertainties in the precision of the FAD and LAD estimates (assumption iv). This phylogeny summarizes current understanding of ancestordescendant relationships among extinct and extant morphospecies based on the work of multiple researchers.…”

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confidence: 99%

“…This phylogeny summarizes current understanding of ancestordescendant relationships among extinct and extant morphospecies based on the work of multiple researchers. It is anchored by a comprehensive compilation of FAD and LAD estimates (24), most of which were obtained using the most precise dating techniques currently available (25)(26)(27). Interpreting this phylogeny in light of molecular evidence for extant members of the Foraminifera (28-31), we calculate upper-bound estimates for the fractions of speciation events that may be the result of anagenesis for the Cenozoic era (last 65 Ma) and for the Neogene period (last 23 Ma), as described in Methods.…”

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confidence: 99%

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Assessing the role of cladogenesis in macroevolution by integrating fossil and molecular evidence

Strotz

Allen

2013

Proc. Natl. Acad. Sci. U.S.A.

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Assessing the extent to which population subdivision during cladogenesis is necessary for long-term phenotypic evolution is of fundamental importance in a broad range of biological disciplines. Differentiating cladogenesis from anagenesis, defined as evolution within a species, has generally been hampered by dating precision, insufficient fossil data, and difficulties in establishing a direct link between morphological changes detectable in the fossil record and biological species. Here we quantify the relative frequencies of cladogenesis and anagenesis for macroperforate planktic Foraminifera, which arguably have the most complete fossil record currently available, to address this question. Analyzing this record in light of molecular evidence, while taking into account the precision of fossil dating techniques, we estimate that the fraction of speciation events attributable to anagenesis is <19% during the Cenozoic era (last 65 Myr) and <10% during the Neogene period (last 23 Myr). Our central conclusion-that cladogenesis is the predominant mode by which new planktic Foraminifera taxa become established at macroevolutionary time scales-differs markedly from the conclusion reached in a recent study based solely on fossil data. These disparate findings demonstrate that interpretations of macroevolutionary dynamics in the fossil record can be fundamentally altered in light of genetic evidence. anagenesis, which occurs within a species, and cladogenesis, which occurs during speciation and results in the subdivision of a species into two reproductively isolated, independently evolving taxa (1, 2). Distinguishing between these modes is essential to determining the role of population subdivision in evolutionary dynamics (3,4). This topic has received considerable attention in paleontology (1, 2), perhaps because the fossil record provides the only direct record of long-term morphological change (5), but its importance extends to other biological disciplines. For example, in population genetics, models only predict that phenotypic change is contingent upon or associated with the evolution of reproductive isolation under specific circumstances (3). Thus, a primary role for cladogenesis may highlight the importance of particular speciation modes (2), metapopulations dynamics (6), or adaptive peaks in fitness landscapes (7,8). In community ecology, both evolutionary modes may influence biodiversity, but the mechanisms differ: only cladogenesis results in an increase in diversity (9-11), but anagenesis may help maintain diversity if it results in niche differences that facilitate species coexistence (12, 13).Remarkably few studies have attempted to quantify the relative frequencies of anagenesis and cladogenesis for entire species assemblages (e.g., refs. 5, 14, 15). Addressing this question is challenging due to insufficient fossil data for most taxa and the difficulties in relating morphological change to genetic divergence and the evolution of reproductive isolation (16). Fossil data can only be used to distinguish anag...

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confidence: 99%

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confidence: 99%

Assessing the role of cladogenesis in macroevolution by integrating fossil and molecular evidence

Strotz

Allen

2013

Proc. Natl. Acad. Sci. U.S.A.

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“…Genetic data (from ∼20 morphospecies) support the simplifying assumption of our study that the vast majority of taxa recognized as distinct morphospecies are reproductively isolated and therefore independently evolving. The one established exception is the recent discovery of genetic homogeneity within the Globigerinoides sacculifer plexus (4), where we recognize two morphs, as per Aze et al (2). This important finding highlights that we still have much to learn about foraminifera diversity, but it does not, by itself, refute our simplifying assumption as appropriate for estimating the relative frequencies of anagenesis and cladogenesis, particularly as it is an example of ecophenotypy, not anagenesis.…”

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confidence: 83%

“…The phylogeny developed by Aze et al (2) forms the basis of our study and represents an important contribution to the field. Aze et al question our methodology (3), but the alternative they advocate, which relies entirely on a lineage-based approach (2), is by itself insufficient to distinguish speciation modes.…”

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confidence: 98%

Reply to Aze et al.: Distinguishing speciation modes based on multiple lines of evidence

Strotz¹,

Allen²

2013

Proc. Natl. Acad. Sci. U.S.A.

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In a recent study, we present evidence that cladogenesis is the primary driver of longterm phenotypic evolution in planktic foraminifera (1). The phylogeny developed by Aze et al. (2) forms the basis of our study and represents an important contribution to the field. Aze et al. question our methodology (3), but the alternative they advocate, which relies entirely on a lineage-based approach (2), is by itself insufficient to distinguish speciation modes.In their response, Aze et al. (3) reiterate that their phylogeny does not incorporate findings from genetic studies to ensure its independence. Consequently, they do not consider evidence that may aid in distinguishing anagenesis from cladogenesis. Contrary to the statement of Aze et al. (3), we never claimed to analyze molecular data; rather, we interpret fossil data in light of molecular and other evidence (1). Genetic data (from ∼20 morphospecies) support the simplifying assumption of our study that the vast majority of taxa recognized as distinct morphospecies are reproductively isolated and therefore independently evolving. The one established exception is the recent discovery of genetic homogeneity within the Globigerinoides sacculifer plexus (4), where we recognize two morphs, as per Aze et al. (2). This important finding highlights that we still have much to learn about foraminifera diversity, but it does not, by itself, refute our simplifying assumption as appropriate for estimating the relative frequencies of anagenesis and cladogenesis, particularly as it is an example of ecophenotypy, not anagenesis.The criteria we use to distinguish speciation modes are not based on "just two studies" (3), but rather a comprehensive review of relevant and available evidence. One form is temporal range overlap for ancestor-descendant pairs (5). We agree that the amount of range overlap is partly "an artifact of the typological approach" for defining morphospecies (3), as we show in figure 2A (1), which is why we account for it in our study. Our typological error estimates-one each for the Neogene and Paleogene-were drawn from detailed studies of 20 speciation events. Given the small sample size (20 of 337 Cenozoic events), we acknowledge here and in our paper the need for further work in this area. Within our typological error margins, all events were assumed to be anagenetic in the absence of other evidence. Because such evidence is currently unavailable for the majority of speciation events within our error margins (57 of 105), our method of identifying cladogenetic events is conservative.As Aze et al. acknowledge (3), many more cladogenetic events have likely occurred than are resolved in their phylogeny. Our methodology was specifically designed to distinguish speciation modes by incorporating other evidence. Because it entails explicit assumptions and is quantitative, it can be modified in light of new findings as they become available. We view our approach as complementary to the lineage-based approach and the detailed morphometric and molecular studies that wil...

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“…Porosity, pore density, and average pore size were examined for a phylogenetic signal by estimating Pagel's lambda using average porosity for each species and the Cenozoic planktonic foraminiferal phylogeny of Aze et al (2011). Pagel's lambda is a test designed to identify statistically significant grouping of trait values in phylogenetic clades as compared to the random 180 distribution expected in the absence of a phylogenetic signal (Pagel, 1999).…”

Section: Testing For Phylogenetic Signalmentioning

confidence: 99%

Factors Influencing Porosity in Planktonic Foraminifera

Burke¹,

Renema²,

Henehan³

et al. 2018

Preprint

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Abstract. The clustering of mitochondria near pores in the test walls of foraminifera suggests that these perforations play a critical role in metabolic gas exchange. As such, pore measurements could provide a novel means of tracking changes in metabolic rate in the fossil record. However, in planktonic foraminifera, variation in pore size, density, and porosity have been 20 variously attributed to environmental, biological, and taxonomic drivers, complicating such an interpretation. Here we examine the environmental, biological, and evolutionary determinants of porosity in 718 individuals representing 17 morphospecies of planktonic foraminifera from 6 core tops in the North Atlantic. Using random forest models, we find that porosity is primarily correlated to size and habitat temperature, two key factors in determining metabolic rates. In order to test if this correlation arose spuriously through the association of cryptic species with distinct biomes, we cultured Globigerinoides ruber in three 25 different temperature conditions, and found that porosity increased with temperature. Crucially, these results show that porosity can be plastic: changing in response to environmental drivers within the lifetime of an individual foraminifer. This demonstrates the potential of porosity as a proxy for foraminiferal metabolic rates, with significance for interpreting geochemical data and the physiology of foraminifera in non-analog environments. It also highlights the importance of phenotypic plasticity (i.e., ecophenotypy) in accounting for some aspects of morphological variation in the modern and fossil 30 record.

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A phylogeny of Cenozoic macroperforate planktonic foraminifera from fossil data

Cited by 222 publications

References 126 publications

Assessing the role of cladogenesis in macroevolution by integrating fossil and molecular evidence

Assessing the role of cladogenesis in macroevolution by integrating fossil and molecular evidence

Reply to Aze et al.: Distinguishing speciation modes based on multiple lines of evidence

Factors Influencing Porosity in Planktonic Foraminifera

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