‘Fish’ (Actinopterygii andElasmobranchii) diversification patterns through deep time

Abstract

Actinopterygii (ray-finned fishes) and Elasmobranchii (sharks, skates and rays) represent more than half of today's vertebrate taxic diversity (approximately 33000 species) and form the largest component of vertebrate diversity in extant aquatic ecosystems. Yet, patterns of 'fish' evolutionary history remain insufficiently understood and previous studies generally treated each group independently mainly because of their contrasting fossil record composition and corresponding sampling strategies. Because direct reading of palaeodiversity curves is affected by several biases affecting the fossil record, analytical approaches are needed to correct for these biases. In this review, we propose a comprehensive analysis based on comparison of large data sets related to competing phylogenies (including all Recent and fossil taxa) and the fossil record for both groups during the Mesozoic-Cainozoic interval. This approach provides information on the 'fish' fossil record quality and on the corrected 'fish' deep-time phylogenetic palaeodiversity signals, with special emphasis on diversification events. Because taxonomic information is preserved after analytical treatment, identified palaeodiversity events are considered both quantitatively and qualitatively and put within corresponding palaeoenvironmental and biological settings. Results indicate a better fossil record quality for elasmobranchs due to their microfossil-like fossil distribution and their very low diversity in freshwater systems, whereas freshwater actinopterygians are diverse in this realm with lower preservation potential. Several important diversification events are identified at familial and generic levels for elasmobranchs, and marine and freshwater actinopterygians, namely in the Early-Middle Jurassic (elasmobranchs), Late Jurassic (actinopterygians), Early Cretaceous (elasmobranchs, freshwater actinopterygians), Cenomanian (all groups) and the Paleocene-Eocene interval (all groups), the latter two representing the two most exceptional radiations among vertebrates. For each of these events along with the Cretaceous-Paleogene extinction, we provide an in-depth review of the taxa involved and factors that may have influenced the diversity patterns observed. Among these, palaeotemperatures, sea-levels, ocean circulation and productivity as well as continent fragmentation and environment heterogeneity (reef environments) are parameters that largely impacted on 'fish' evolutionary history, along with other biotic constraints.

Contrasting “Fish” Diversity Dynamics between Marine and Freshwater Environments

“…In a previous study [16], we provided a range of computed diversity values according to the various phylogenies considered and their corresponding congruence with the fossil record, indicating that genuine diversity values should lie within this range. Consequently, the median diversity value was selected here for each time bin in order to sum up all hypotheses in one curve.…”

“…As specialization reduces direct competition by subdividing ecospaces, competition may favor increasing adaptative evolution and speciation [35], particularly in restricted or isolated environments. In addition to exhibiting greater isolation, specialization, and competition, freshwater fish groups appear less affected by extinction events at the family level in comparison with marine clades [16], which may explain parts of the differential diversity dynamics observed. This might relate to the different structure of these ecosystems, with the marine biota from the photic zone being based on primary producers and zooplankton whereas freshwater ecosystems also largely rely on detrital food webs.…”

“…Tectonics, and to a greater extent the evolution of Earth's geographical and environmental configuration, are another factor that may explain the contrasting deep-time evolution of the freshwater and marine ''fish'' diversities. The Mesozoic-Cenozoic interval is characterized mainly by the breakup of Pangaea, which provided increasing ecological niches in both marine and continental ecosystems [16]. In the marine realm, it has been shown that periods of high sea levels coupled with warm global temperatures (Upper Cretaceous, Paleocene-Eocene) are linked with major diversification events within ''fishes'' [16] and more broadly vertebrates [15], along with habitat complexification related to the settlement of modern reef ecosystems (Paleocene-Eocene).…”

Little evidence for enhanced phenotypic evolution in early teleosts relative to their living fossil sister group

“…This perspective became enshrined in mid-20th century treatments of actinopterygian evolution, which recognized an early-mid Mesozoic phase dominated by holosteans sensu lato and a later interval, extending to the modern day, dominated by teleosts (4,20,21). Contemporary paleontological accounts echo the classic interpretation of modest teleost origins (22)(23)(24), despite a systematic framework that substantially revises the classifications upon which older scenarios were based (22)(23)(24)(25). Identification of explosive lineage diversification in nested teleost subclades like otophysans and percomorphs, rather than across the group as a whole, provides some circumstantial neontological support for this narrative (26).…”

“…In contrast to quantified taxonomic patterns (20,23,24,27), phenotypic evolution in early neopterygians has only been discussed in qualitative terms. The implicit paleontological model of morphological conservatism among early teleosts contrasts with the observation that clades aligned with the teleost stem lineage include some of the most divergent early neopterygians in terms of both size and shape ( Fig.…”