Climate cooling and clade competition likely drove the decline of lamniform sharks

Abstract

Understanding heterogeneity in species richness between closely related clades is a key research question in ecology and evolutionary biology. Multiple hypotheses have been proposed to interpret such diversity contrasts across the tree of life, with most studies focusing on speciation rates to explain clades’ evolutionary radiations, while often neglecting extinction rates. Here we study a notorious biological model as exemplified by the sister relationships between mackerel sharks (Lamniformes, 15 extant species) and ground sharks (Carcharhiniformes, ∼290 extant species). Using a comprehensive fossil dataset, we found that the diversity dynamics of lamniforms waxed and waned following repeated cycles of radiation phases and declining phases. Radiation phases peaked up to 3 times the current diversity in the early Late Cretaceous. In the last 20 million years, the group declined to its present-day diversity. Along with a higher extinction risk for young species, we further show that this declining pattern is likely attributed to a combination of abiotic and biotic factors, with a cooling-driven extinction (negative correlation between temperature and extinction) and clade competition with some ground sharks. Competition from multiple clades successively drove the demise and replacement of mackerel sharks due to a failure to originate facing the rise of ground sharks, particularly since the Eocene. These effects came from ecologically similar carcharhiniform species inhibiting diversification of medium- and large-sized lamniforms. These results imply that the interplay between abiotic and biotic drivers had a substantial role in extinction and speciation, respectively, which determines the sequential rise and decline of marine apex predators.

Diversity and renewal of tropical elasmobranchs around the Middle Eocene Climatic Optimum (MECO) in North Africa: New data from the lagoonal deposits of Djebel el Kébar, Central Tunisia

“…In that context, these two localities from central-West Tunisia testify a deep change in tropical shark communities during the Middle Eocene with post-Lutetian dominance of Carcharhiniformes compared to the early Paleogene where Lamniformes and Orectolobiformes were comparitively as well represented in Tunisia and Morocco for instance (Arambourg, 1952;Noubhani and Cappetta, 1997). This local trend also prefigures the worldwide decline of Lamniformes after the Paleogene in favour of the medium-large Carcharhiniformes (e.g., requiem and hammerhead sharks), which increased since the Eocene (Condamine et al, 2019).…”

Distinct Responses of Elasmobranchs and Ray-Finned Fishes to Long-Term Global Change

“…We found that marine actinopterygian diversity correlates strongly negatively with δ 18 O values, which are considered as an inverse proxy for global climate change that mainly reflects temperature fluctuations (also global ice volume during icehouse periods) (Zachos et al, 2008). The positive link between temperature and diversity has probably been the most widely recovered relationship in macroevolutionary studies on both marine and terrestrial groups and across many lineages (Aguirre and Riding, 2005;Hunt et al, 2005;Marx and Uhen, 2010;Ezard et al, 2011;Figueirido et al, 2012;Mayhew et al, 2012;Condamine et al, 2013Condamine et al, , 2019Martin et al, 2014;De Blasio et al, 2015;Mannion et al, 2015). Temperature is also recognized as acting on the spatial distribution of biodiversity in modern ecosystems through the latitudinal diversity gradient (Willig et al, 2003;Hillebrand, 2004;Tittensor et al, 2010).…”

“…This temperature-sensitive trait may partly explain the stronger effect of climate on actinopterygian diversity than on elasmobranchs, which produce less egg cases (or youngs per liters) and have no larval or free egg phases. However, a recent species-level analysis provided evidence that lamniform extinction rates were negatively correlated with temperature (Condamine et al, 2019), which indicates that this parameter also played a role in some clades of mostly pelagic elasmobranchs.…”

“…Based on our results, it is expected that results found in such Phanerozoic marine invertebrate analyses are unbalanced by dominant ecologies among marine invertebrates and that the real patterns of abiotic control on deep-time biodiversity variations are more complex than previously expected. Although this is a first step in the understanding of what shapes the evolutionary history of clades, biotic interactions including competition (Liow et al, 2015;Silvestro et al, 2015;Voje et al, 2015) and predation (Huntley and Kowalewski, 2007;Marx and Uhen, 2010) have been more scarcely tested but have been demonstrated to play a role in the diversification patterns of clades, including sharks (Condamine et al, 2019). Exploring these intrinsic biotic effects represent another challenge for future studies, as is the understanding of the long-term drivers of continental fish diversity.…”

“…These studies mainly focused on marine invertebrate data (Mayhew et al, 2008(Mayhew et al, , 2012Cárdenas and Harries, 2010;Ezard et al, 2011;Hannisdal and Peters, 2011;Liow et al, 2015), whereas those that explored the role of some environmental variations over marine or continental vertebrate clades are comparatively scarce and concern low-diversity tetrapod groups (Marx and Uhen, 2010;Benson and Butler, 2011;Butler et al, 2011;Martin et al, 2014;Mannion et al, 2015). Multiple lines of evidence indicate that temperature acted as a major control over the evolutionary history of clades (Aguirre and Riding, 2005;Hunt et al, 2005;Marx and Uhen, 2010;Ezard et al, 2011;Figueirido et al, 2012;Mayhew et al, 2012;Condamine et al, 2013Condamine et al, , 2019Martin et al, 2014;De Blasio et al, 2015;Mannion et al, 2015), but it has been demonstrated that other factors such as sea-level (Peters, 2005;Benson and Butler, 2011;Hannisdal and Peters, 2011), tectonics (Zaffos et al, 2017), and nutrient availability (Cárdenas and Harries, 2010) likely acted over the evolution of biodiversity.…”