Shark mandible evolution reveals patterns of trophic and habitat-mediated diversification

Abstract

Environmental controls of species diversity represent a central research focus in evolutionary biology. In the marine realm, sharks are widely distributed, occupying mainly higher trophic levels and varied dietary preferences, mirrored by several morphological traits and behaviours. Recent comparative phylogenetic studies revealed that sharks present a fairly uneven diversification across habitats, from reefs to deep-water. We show preliminary evidence that morphological diversification (disparity) in the feeding system (mandibles) follows these patterns, and we tested hypotheses linking these patterns to morphological specialisation. We conducted a 3D geometric morphometric analysis and phylogenetic comparative methods on 145 specimens representing 90 extant shark species using computed tomography models. We explored how rates of morphological evolution in the jaw correlate with habitat, size, diet, trophic level, and taxonomic order. Our findings show a relationship between disparity and environment, with higher rates of morphological evolution in reef and deep-water habitats. Deep-water species display highly divergent morphologies compared to other sharks. Strikingly, evolutionary rates of jaw disparity are associated with diversification in deep water, but not in reefs. The environmental heterogeneity of the offshore water column exposes the importance of this parameter as a driver of diversification at least in the early part of clade history.

Evolutionary trends in the elasmobranch neurocranium

“…In teleosts, the maxilla and premaxillar are highly kinetic and the upper jaw and suspensorium can be tightly connected to the braincase. By contrast the elasmobranch cranium is uniquely decoupled, with a few, often highly kinetic skeletal connections between the braincase and jaws 39 , 40 , 47 – 49 . Thus we might predict that elasmobranch neurocranial geometry may have a different degree of correlation with diet.…”

“…In Selachii the jaws are articulated to the braincase through the hyomandibular cartilages and a suspensory ligament joining the anterior neurocranium to the palatoquadrate 63 , 64 . In batoids this ethmopalatine ligament is lost 47 , 65 , meaning that the otic region of the neurocranium is more important to jaw articulation in batoids than in selachians. The loss of this ligamentous connection may thus have increased the functional separation of the otic and occipital regions of the batoid neurocranium.…”

“…In this scenario, increased modularity between the otic and occipital regions is adaptive as it overcomes constraint imposed by subunits of a morphological structure that differ functionally. As a result, batoids have far greater motor control in the feeding apparatus and have evolved many innovations to the hyomandibular musculature to facilitate specialisation 5 , 47 , 65 , 66 which may not have been possible in the absence of some degree of evolutionary independence between the occipital and otic regions. The loss of the ethmopalatine ligament would also likely have released the rostrum from evolutionary constraint, enabling greater optimisation of hydrodynamic function and the evolution of novel, batoid-specific roles in prey acquisition 37 .…”

The origins and drivers of sexual size dimorphism in sharks

“…It is generally accepted that ecological selection acts on body size in vertebrates (Blanckenhorn, 2000 ; Sheridan & Bickford, 2011 ; Shine, 1989 ), and that in some systems, SSD reflects a balance or trade‐off between natural selection and sexual selection (Nudds & Kaminski, 1984 ; Pearson et al., 2002 ; Shine, 1989 ; Wikelski & Trillmich, 1997 ). We used depth as a measure of ecology as the shallow‐deep continuum is known to have been an influential force shaping morphological evolution in elasmobranchs (López‐Romero et al., 2023 ; Sorenson et al., 2014 ), and it is generally recognised that the complexity and diversity of shallow‐water marine environments (Martinez et al., 2021 ; Miller et al., 2022 ) leads to a gradient of relatively weak to strong ecological selection with increasing depth. In shallow‐water environments, greater ecological complexity and higher competition levels could favour enhanced niche/resource partitioning (Cloyed & Eason, 2017 ), in turn favouring the evolution of stronger SSD, which could be either female or male‐biased depending on the system in question.…”

Evolutionary trends in the elasmobranch neurocranium

“…The most notable difference between our results and those recovered from other vertebrates is the absence of any signi cant relationship between neurocranium geometry and diet (Table 1). In other groups prey acquisition/handling is thought to be amongst the most signi cant selective pressures acting throughout the cranium, and as a result neurocranium shape frequently correlates with aspects of diet and trophic ecology (2,(41)(42). In this regard the elasmobranch cranium displays mosaic evolution, where different parts of the skull show contrasting patterns of ecological signal.…”