The early diversification of ray-finned fishes (Actinopterygii): hypotheses, challenges and future prospects

Abstract

Actinopterygii are the most speciose living vertebrate clade, and study of fossil members during their Palaeozoic rise to dominance has a long history of descriptive work. Although research interest into Palaeozoic actinopterygians has increased in recent years, broader patterns of diversity and diversity dynamics remain critically understudied. Past studies have investigated macroevolutionary trends in Palaeozoic actinopterygians in a piecemeal fashion, variably using existing compendia of vertebrates or literature-based searches, and there is no comprehensive occurrence-based dataset of actinopterygians spanning the whole of the Palaeozoic. Past studies typically show low levels of diversity in the Devonian with a substantial rise in the early Carboniferous in the aftermath of the end-Devonian mass extinction. However there are unresolved patterns reported for the later Carboniferous and Permian. In large part, these conflicts span from a lack of publicly-available occurrence data: actinopterygians are majorly underrepresented in the Paleobiology Database (PBDB), for example, obscuring patterns of diversity through time. This is exacerbated by major taxonomic problems pervading the Palaeozoic actinopterygian record. Innumerable taxa are lumped into wide-ranging families and poorly-formulated genera, with a vast number of described species concentrated in several particularly problematic ‘waste-basket’ genera. This taxonomic confusion feeds into a limited understanding of phylogenetic relationships. There is also a heavy sampling bias towards Europe and North America, with other regions underrepresented despite yielding important occurrences. Scrutiny of the extent to which spatial biases influence the record is lacking, as is research on other forms of bias. Low richness in some time periods may be linked to geological biases, while the effect of taphonomic biases on Palaeozoic actinopterygians have not yet been investigated. Efforts are already underway to both redescribe poorly defined taxa and describe taxa from underrepresented regions, helping address taxonomic issues and accuracy of occurrence data. New methods of sampling standardisation utilising up-to-date occurrence databases will be critical in teasing apart biological changes in diversity from those resulting from bias. Lastly, continued phylogenetic work will enable the use of phylogenetic comparative methods to elucidate the origins of actinopterygian biogeography and subsequent patterns of radiation throughout their rise to dominate aquatic faunas.

Sampling biases obscure the early diversification of the largest living vertebrate group

“…In contrast to coverage-rarefied diversity estimates, extrapolated estimates from squares analysis return very similar trends to face-value counts of richness (3,5,9). These differences persist regardless of whether sampling is via equal length intervals or geological stages and are likely due to taxonomic biases (see below).…”

“…Changes in local richness largely track changes in ‘global’ (gamma) raw diversity (9), with the exception of the latest Carboniferous and earliest Permian (figure 1). In the late Carboniferous and early Permian, high levels of sampling (localities and equal-area grid cells (9)) of isolated localities with low alpha diversity drives high ‘global’ diversity, with few contributions from diverse assemblages. These richness patterns are drastically different to those reported for Palaeozoic tetrapods (28), and the overall decrease from the Carboniferous to Permian contrasts the biodiversification of invertebrates over the same period (55).…”

“…Certain regions are notably underrepresented throughout the Palaeozoic, such as the northern, eastern and southern Palaeotethys (present-day Middle East, south and east Asia, north Africa) and the northern coastline of Laurussia (present-day Siberia, Kazakhstan and interior of Asia). Sampling through much of the Devonian and Carboniferous is limited to a narrow band around the palaeoequator, largely corresponding to present-day Europe and North America (figure 2), which also contain localities with the highest local richness (9). The most diverse localities trend from low-to mid-palaeolatitudes through the Palaeozoic, essentially tracking the migration of North America and Europe (figure 1b).…”

“…Ray-finned fishes originated in the Palaeozoic, which saw major evolutionary events and changes in the vertebrate fauna, such as the emergence of jaws (2), the rise of actinopterygians (3), and the move onto land (4). Despite these pivotal changes, and a long history of research on actinopterygians, there are relatively few macroevolutionary studies investigating diversity trends in their early evolution, and all examine face-value patterns of taxonomic richness (3,(5)(6)(7)(8)(9).…”

High lineage survivorship across the end-Devonian Mass Extinction suggested by a remarkable new Late Devonian actinopterygian

“…Timing of divergences among early actinopterygians in past studies is either taken at face-value from the fossil record (3, 13) or depicted graphically in trees (19, 54, 55) timescaled using naïve a posteriori approaches that impose user-defined branch minima or redistribute branch lengths among clades (56). Prevailing hypotheses using these approaches posit that a minimal number of lineages crossed the end-Devonian boundary, with explosive diversification occurring in the early Carboniferous.…”