Oceans blanket more than two-thirds of Earth's surface, yet marine biodiversity is disproportionately concentrated in coral reefs. Investigating the origins of this exceptional diversity is crucial for predicting how reefs will respond to anthropogenic disturbances. Here, we use a genome-scale dataset to reconstruct the evolutionary history of the wrasses and parrotfishes (Labridae), which rank among the most species-rich and ecologically diverse lineages of reef fishes. We show that major labrid clades experienced pulses of evolutionary innovation and accelerated diversification during the Miocene approximately 20 to 15 million years ago that the origin of no single phenotypic trait can explain. These results draw parallels to the evolutionary histories of many clades after mass extinctions and corroborate recent fossil evidence for an Early Miocene extinction event in oceanic vertebrates and changes in coral reef faunal composition. Our data provide genomic evidence for a major Early Miocene reassembly of reef faunas.

The primary function of the vertebrate jaw is the dorsoventral movement that occurs during opening and closing. Yet, several lineages have evolved the ability to move their jaws laterally, enabling major innovations, like chewing. While lateral jaw motions are primarily known in tetrapods, here, we show that an ecologically dominant lineage of reef fishes (Zanclidae and Acanthuridae) has evolved the ability to laterally rotate their jaws during feeding. This unique function substantially expands both the kinematic versatility and known diversity of vertebrate jaw mechanisms, adding to the growing list of innovations that followed the origin of jaws. Within Acanthuridae, this increased kinematic versatility may allow for algal detachment with minimal movement of the rest of the body, facilitating rapid biting within the same microtopographic location, and thus, this lineage having the highest bite rates among biting reef fishes. This innovation may have thus helped create one of the most ecologically diverse and speciose herbivorous reef fish lineages. Our results highlight the ecological and evolutionary impact of lateral jaw rotation within vertebrates, and potentially how this novelty led to a significant change in coral reef trophodynamics.

Rates of lineage diversification vary considerably across the tree of life, often as a result of evolutionary innovations1-5. Although the ability to produce new traits can vary between clades and may drive ecological transitions6-9, the impact of differences in the pace at which innovations evolve at macroevolutionary scales has been overlooked. Complex teeth are one innovation that contributed to the evolutionary success of major vertebrate lineages10-12. Here we show that evolutionary lability of tooth complexity, but not complexity itself, spurs rapid diversification across ray-finned fishes. Speciation rates are five times higher when transitions between simple and complex teeth occur rapidly. We find that African cichlids are unique among all fishes; they are dominated by lineages that transition between simple and complex teeth at unparalleled rates. This innovation interacted with the ecological versatility of complex teeth to spur rapid adaptive radiations in lakes Malawi, Victoria and Barombi Mbo. The marked effect on diversification stems from the tight association of tooth complexity with microhabitat and diet. Our results show that phylogenetic variation in how innovations evolve can have a stronger effect on patterns of diversification than the innovation itself. Investigating the impact of innovations from this new perspective will probably implicate more traits in causing heterogeneous diversification rates across the tree of life.

Sex-specific behaviours are common across animals and often associated with sexual dimorphism in the nervous system. Using micro-CT scanning we standardized sex-specific brain atlases and tested for sexual dimorphism in the brain of the orchid bee Euglossa dilemma, a species with marked sex differences in social behaviour, mating strategies and foraging. Males show greater investment in all primary visual processing neuropils and are uniquely integrated with the central complex, evidenced by a strong positive covariation. This suggests that males invest more on locomotor control, flight stability and sky-compass navigation which may have evolved in response to sex-specific behaviours, like courtship display. In contrast, females have larger mushroom bodies that strongly and positively covary with the optic lobes and have increased volume of the Kenyon cell cluster, implying greater capabilities for visual associative memory. We speculate this is an adaptation to social and nest-building behaviours, and reliance on learning visual landmarks required for central place foraging. Our study provides the first record of sexually dimorphic morphological integration in the brain of an insect, an approach that revealed sex-specific brain traits that lack an apparent morphological signal. These subtle differences provide further evidence for the causal link between brain architecture and behaviour.

Innovations often shape the trajectory of macroevolution, yet their effects are usually considered independently, thus ignoring the functional and evolutionary interactions between them. Two innovations that have underpinned the ecological and evolutionary success of ray-finned fishes (Actinopterygii) are large teeth and highly protrusible jaws, which independently expanded the diversity of prey capture strategies. Here, we explore the functional relationship between these innovations across actinopterygians using high-speed videography and phylogenetic comparative methods. We find that these two innovations are functionally and evolutionarily incompatible because there is an overarching tradeoff between jaw protrusion and tooth size. Having large teeth decreases the kinematic diversity of prey capture by restricting species to overtake prey predominantly by swimming, while highly protrusible jaws are only found in species with small teeth. The space within tooth-bearing bones may impose this constraint, by limiting the maximum tooth size of species with gracile jaws adapted for high mobility and jaw protrusion. Nevertheless, some species break this constraint on tooth size through novel adaptations that accommodate exceptionally large teeth, unlocking new feeding modes which may have expanded the nature of aquatic feeding and influenced the ecosystems themselves. Although both high jaw protrusion and large teeth separately expanded prey capture strategies in fishes, they are generally not found in combination and are evolutionarily incompatible.

Adaptive radiations highlight the mechanisms by which species and traits diversify and the extent to which these patterns are predictable. We used 1,110 high-speed videos of suction feeding to study functional and morphological diversification in 300 cichlid species from three African Great Lake radiations of varying ages (Victoria, Malawi, and Tanganyika) and an older, spatially dispersed continental radiation in the Neotropics. Among African radiations, standing diversity was reflective of time. Morphological and functional variance in Lake Victoria, the youngest radiation, was a subset of that within Lake Malawi, which itself was nested within the older Tanganyikan radiation. However, functional diversity in Neotropical cichlids was often lower than that in Lake Tanganyika, despite being much older. These two radiations broadly overlapped, but each diversified into novel trait spaces not found in the youngest lake radiations. Evolutionary rates across radiations were inversely related to age, suggesting extremely rapid trait evolution at early stages, particularly in lake radiations. Despite this support for early bursts, other patterns of trait diversity were inconsistent with expectations of adaptive radiations. This work suggests that cichlid functional evolution has played out in strikingly similar fashion in different radiations, with contingencies eventually resulting in lineage-specific novelties.

Anglerfish are creatures of the deep ocean, featuring glowing lures, huge, toothy mouths and parasitic males physically attached to females. A new study finds that genomic degradation of the immune system facilitated the origin of parasitic males as anglerfishes invaded the deep zone where they experienced an adaptive radiation.

Modifications to the pharyngeal jaws-a prey processing system located posterior to the mouth cavity-are widely considered a key innovation that enhanced diversification within several prominent fish clades. Seen in cichlids, damselfishes, wrasses, and a few other lineages, these musculoskeletal alterations are believed to increase the evolutionary independence and, thus, the diversification of the oral and pharyngeal jaw systems. To test this classic hypothesis, we conducted comparative phylogenetic analyses to assess the effect of the pharyngeal novelty on the diversification of feeding morphology and kinematics across a taxonomically diverse sample of spiny-rayed fishes. We quantified movements of the oral jaws and other craniofacial structures from 689 suction-feeding strikes using high-speed videos collected from 228 species with and without the pharyngeal jaw novelty. Contradicting long-held predictions, we find significantly greater disparity across all traits and faster rates of oral jaw functional evolution in fishes without the specialized prey processing system. The modified pharyngeal jaw is undoubtedly a functional innovation as it enhances the strength of the prey processing system, facilitating exceptional transition rates to feeding on hard and tough prey. However, it also restricts the diversification of the feeding system, revealing that the impact of pharyngognathy is more nuanced than previously thought. In light of these and other recent findings, a reinterpretation of the macroevolutionary consequences of the pharyngeal jaw novelty is needed. Modifications to the pharyngeal jaws-a prey processing system located posterior to the mouth cavity-are widely considered a key innovation that enhanced diversification within several prominent fish clades. Seen in cichlids, damselfishes, wrasses, and a few other clades, these musculoskeletal alterations are believed to increase the evolutionary independence and, thus, the diversification of the oral and pharyngeal jaw systems. To test this classic hypothesis, we used comparative phylogenetic analyses to examine the diversification of oral jaw morphology and feeding motions in 228 fish species, including 133 and 95 taxa with and without modified pharyngeal jaws, respectively. Contradicting long-held predictions, we reveal that the novelty restricts the diversification of the feeding system overall despite enhancing the functional capacity of the pharyngeal jaws. Our findings highlight the importance of examining the consequences of specialized traits within a comparative framework, as their presence may not be uniformly advantageous to the diversification of functional systems. Thousands of fish species inhabit diverse aquatic environments due, in part, to the evolution of functional innovations. Such traits enable novel interactions with the environment, often facilitating increased diversification within the lineages in which they occur. Modifications to the pharyngeal jaws-a second jaw system located behind the mouth cavity that primarily functions to process prey-are widely considered innovations as multiple musculoskeletal changes allow fishes to process harder and tougher prey items (e.g., mollusks, algae). These modifications to the prey processing apparatus are predicted to increase the independence of the oral and pharyngeal jaws, enabling greater morphological and functional diversification in both systems. To test this classic hypothesis, we examined the diversification of oral jaw morphology and feeding motions in fishes with the modified pharyngeal jaw (133 species representing 4 families) and those without it (95 species representing 39 families). Contrary to long-held predictions, fishes with a specialized prey processing system show less variance across all traits and slower rates of functional evolution. Thus, although the novelty enhances the functional capacity of the pharyngeal jaws, it is also associated with restricted diversification of the feeding system. Our results highlight the importance of examining the consequences of specialized traits within a comparative framework, as their presence may not be uniformly advantageous to the diversification of functional systems.

Major trade-offs often manifest as axes of diversity in organismal functional systems. Overarching trade-offs may result in high trait integration and restrict the trajectory of diversification to be along a single axis. Here, we explore the diversification of the feeding mechanism in coral reef fishes to establish the role of trade-offs and complexity in a spectacular ecological radiation. We show that the primary axis of variation in the measured musculo-skeletal traits is aligned with a trade-off between mobility and force transmission, spanning species that capture prey with suction and those that bite attached prey. We found weak or no covariation between about half the traits, reflecting deviations from the trade-off axis. The dramatic trophic range found among reef fishes occurs along the primary trade-off axis, with numerous departures that use a mosaic of trait combinations to adapt the feeding mechanism to diverse challenges. We suggest that morphological evolution both along and independent of a major axis of variation is a widespread mechanism of diversification in complex systems where a global trade-off shapes major patterns of diversity. Significant additional diversity emerges as systems use weak integration and complexity to assemble functional units with many trait combinations that meet varying ecological demands. The diversity of coral reef fishes' feeding apparatus aligns with the trade-off between mobility and force transmission, but weak trait covariation and complexity allow jaw traits to evolve independently to adapt to diverse ecological challenges.

In functional systems composed of many traits, selection for specialized function can induce trait evolution by acting directly on individual components within the system, or indirectly through networks of trait integration. However, strong integration can also hinder diversification into regions of trait space that are not aligned with axes of covariation among traits. Thus, non-independence among traits may limit functional expansion. We explore this dynamic in the evolution of fin shapes in 106 species from 38 families of coral reef fishes, a polyphyletic assemblage that shows exceptional diversity in locomotor function. Despite expectations of a strong match between form and function, we find subtantial fin shape disparity across species that share a swimming mode. The evolution of fin shape is weakly integrated across the four functionally dominant fins in swimming and integration is weakened as derived swimming modes evolve. The weak integration among fins in the ancestral locomotor condition provides a primary axis of diversification while allowing for off-axis diversification via independent trait responses to selection. However, the evolution of novel locomotor modes coincides with a loss of integration among fins. Our study highlights the need for additional work on the functional consequences of fin shape in fishes.