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

Abstract

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...

Can Modern Evolutionary Theory Explain Macroevolution?

“…(Well, maybe.) Although this model is not the only one that might account for a correlation between divergence and speciation (Rabosky 2012), the evidence mentioned earlier (e.g., Mattila and Bokma 2008;Venditti and Pagel 2010;Strotz and Allen 2013) is consistent with it. So is evidence suggesting a break between intraspecific evolution and divergence between reproductively isolated populations.…”

“…Although punctuated gradualism has been claimed for some lineages of planktonic Foraminifera, which provide exceptionally complete fossil records (e.g., Malmgren et al 1983), Gould and Eldredge (1993) claimed that many studies find temporal overlap, supporting their model. A recent comprehensive analysis of 337 Cenozoic "speciation" events in Foraminifera concluded that at most 19 % of Cenozoic events (last 65 million years) and 10 % of Neogene events (last 23 million years) represented change within nondividing lineages: The great majority revealed temporal overlap, and hence biological speciation (Strotz and Allen 2013). Analyses of living species can also shed light on the question.…”

Tachypleus syriacus (Woodward)—a sexually dimorphic Cretaceous crown limulid reveals underestimated horseshoe crab divergence times

“…The combination of fossil and molecular data has the potential to form a powerful toolkit with which to tackle longstanding macroevolutionary issues (Strotz and Allen 2013;Garwood et al 2014;Longrich et al 2015). Fossils represent a unique information resource that can be invaluable for informing on patterns of biogeography, recognizing patterns of character acquisition, and inferring the timing of divergences.…”

A new tyrannosaur with evidence for anagenesis and crocodile-like facial sensory system

“…For paleontologists, the best evidence for anagenesis requires dense stratigraphic sampling and precise radiometric dating, temporally successive specimens of close phylogenetic relationship, clear stratigraphic data for specimens, and a high sample size that includes growth series11819202425. Tyrannosaurs represent one of the few dinosaur clades that meet these criteria7262728.…”