Periodic Reporting for period 2 - MYSTICETI (The oldest and the rarest - combining insight from both hemispheres to gain a global picture of baleen whale origins and macroevolution)
Reporting period: 2017-11-16 to 2018-11-15
Cetaceans (whales and dolphins) are a spectacular example of secondary adaptation of vertebrates to aquatic life. Whales, in particular, are the largest animals on Earth, and play key ecological roles as ecosystem engineers. They owe their success to their highly specialised and efficient way of feeding: unlike most other mammals, whales have no teeth, and instead use baleen – an array of comb-like plates suspended from their upper jaws – to filter vast quantities of tiny prey directly from seawater. How filter feeding evolved, and what role it played in whale evolution, remains a key questions of marine mammal evolution.
This project combines cutting-edge techniques with functional, behavioural, molecular and morphological observations to investigate how, when and why whales whales acquired their unique filter feeding strategy, and what role this transition played in making them the leviathans we know today.
Historically, the study of marine mammals has often focused on species and fossils from the Northern Hemisphere, reflecting its longer history of research and higher population density. To obtain a more global data set, this project specifically focuses on previously undersampled areas, animals and time periods. These include major Southern Hemisphere localities in Australia, New Zealand and Peru, all of which have yielded numerous, yet still largely undescribed fossils; the enigmatic pygmy right whale, Caperea marginata, which is the smallest of the living whales, and only occurs in southern seas; and the earliest phase of whale evolution, lasting from ca 35 to 25 million years.
This project combines cutting-edge techniques with functional, behavioural, molecular and morphological observations to investigate how, when and why whales whales acquired their unique filter feeding strategy, and what role this transition played in making them the leviathans we know today.
Historically, the study of marine mammals has often focused on species and fossils from the Northern Hemisphere, reflecting its longer history of research and higher population density. To obtain a more global data set, this project specifically focuses on previously undersampled areas, animals and time periods. These include major Southern Hemisphere localities in Australia, New Zealand and Peru, all of which have yielded numerous, yet still largely undescribed fossils; the enigmatic pygmy right whale, Caperea marginata, which is the smallest of the living whales, and only occurs in southern seas; and the earliest phase of whale evolution, lasting from ca 35 to 25 million years.
This project has resulted in the discovery of several new species of extinct baleen whales (Mysticeti) from Antarctica, Australia, Peru and Europe, all of which were placed into comprehensive phylogenetic analyses combining anatomical and genetic data. In addition, we produced new observations on pygmy right whales, a rare and enigmatic family represented today by just a single species (Caperea marginata). These included descriptions of (i) their auditory anatomy, to determine hearing abilities and evolutionary relationships; (ii) a new fossil from Australia, cementing the likely origin of the family in the Southern Hemisphere; and (iii) the first and only fossils from the Northern Hemisphere.
To test whether extant animal behaviour can inform evolutionary patterns, we produced a comprehensive review of the feeding behaviours of living marine mammals. From this emerged a novel framework in which feeding strategies form an evolutionary continuum, leading from semi-aquatic to raptorial, suction, and - ultimately - filter feeding. This continuum arises from a variety of physical and biological factors, and provides an independent source of evolutionary data that can be tested against the fossil record. Applied to baleen whales, our framework suggests that ancient mysticetes first transitioned from tooth-based raptorial to suction feeding, and only later acquired the ability to filter feed on small prey using baleen.
Fossil data provide direct evidence of feeding evolution, as shown by our description of an exceptionally preserved specimen of the cetotheriid Piscobalaena nana, and our report of horizontal wear features in a member of an archaic whale family (Aetiocetidae) previously thought to possess both teeth and baleen. Horizontal wear indicates front-to-back transport of food items inside the mouth, which is more consistent with suction than raptorial or filter feeding. Similar wear occurs in several specimens from Australia, and suggests that suction may indeed have preceded the evolution of filter feeding in whales. This pattern is consistent with our behavioural framework, and further supported by the apparent absence of baleen in the archaic toothed mysticete Llanocetus.
One prominent hypothesis holds that early whales strained prey from water using complex teeth, as seen in living filtering feeding seals. To test this idea, we developed a novel technique to measure tooth shape and sharpness. We found that the teeth of filter feeding seals are blunt, with wide notches that facilitate the passage of water. By contrast, those of early whales are sharp, with narrows notches that restrict water flow. We conclude that early whales did not filter with their teeth, and instead used them to grasp and slice larger food items. Teeth were later lost during an intermediate phase of suction feeding (consistent our behavioural framework), following which baleen evolved as a way to trap small prey.
Finally, we investigated the relationship between feeding evolution and mysticete body size. Our analysis of the archaic mysticete Llanocetus shows that whales grew large more than once during their evolutionary history, even before the origin of baleen. In general, however, larger body size appears to have been associated with the emergence of filter feeding, as in other marine vertebrates. Following a turnover event around 20-23 million years ago, archaic toothed mysticetes disappeared, and only filter feeding species remained. Nevertheless, most whales remained comparatively small, perhaps around 6 m long. New fossils from Italy and Peru show that true gigantism arose slowly, but steadily, from this time onwards, and finally became dominant around 3 million years ago, when most ‘small’ mysticetes went extinct in response to Northern Hemisphere glaciation.
To test whether extant animal behaviour can inform evolutionary patterns, we produced a comprehensive review of the feeding behaviours of living marine mammals. From this emerged a novel framework in which feeding strategies form an evolutionary continuum, leading from semi-aquatic to raptorial, suction, and - ultimately - filter feeding. This continuum arises from a variety of physical and biological factors, and provides an independent source of evolutionary data that can be tested against the fossil record. Applied to baleen whales, our framework suggests that ancient mysticetes first transitioned from tooth-based raptorial to suction feeding, and only later acquired the ability to filter feed on small prey using baleen.
Fossil data provide direct evidence of feeding evolution, as shown by our description of an exceptionally preserved specimen of the cetotheriid Piscobalaena nana, and our report of horizontal wear features in a member of an archaic whale family (Aetiocetidae) previously thought to possess both teeth and baleen. Horizontal wear indicates front-to-back transport of food items inside the mouth, which is more consistent with suction than raptorial or filter feeding. Similar wear occurs in several specimens from Australia, and suggests that suction may indeed have preceded the evolution of filter feeding in whales. This pattern is consistent with our behavioural framework, and further supported by the apparent absence of baleen in the archaic toothed mysticete Llanocetus.
One prominent hypothesis holds that early whales strained prey from water using complex teeth, as seen in living filtering feeding seals. To test this idea, we developed a novel technique to measure tooth shape and sharpness. We found that the teeth of filter feeding seals are blunt, with wide notches that facilitate the passage of water. By contrast, those of early whales are sharp, with narrows notches that restrict water flow. We conclude that early whales did not filter with their teeth, and instead used them to grasp and slice larger food items. Teeth were later lost during an intermediate phase of suction feeding (consistent our behavioural framework), following which baleen evolved as a way to trap small prey.
Finally, we investigated the relationship between feeding evolution and mysticete body size. Our analysis of the archaic mysticete Llanocetus shows that whales grew large more than once during their evolutionary history, even before the origin of baleen. In general, however, larger body size appears to have been associated with the emergence of filter feeding, as in other marine vertebrates. Following a turnover event around 20-23 million years ago, archaic toothed mysticetes disappeared, and only filter feeding species remained. Nevertheless, most whales remained comparatively small, perhaps around 6 m long. New fossils from Italy and Peru show that true gigantism arose slowly, but steadily, from this time onwards, and finally became dominant around 3 million years ago, when most ‘small’ mysticetes went extinct in response to Northern Hemisphere glaciation.
This project has notably increased our knowledge of whale diversity, and shed new light on the most enigmatic of the living species, the pygmy right whale Caperea marginata. Our results demonstrate that Caperea has one of the highest low frequency hearing limits of any mysticete, adding to the impression of a highly specialised species that is unlike any of its peers. We also provide further support for the grouping of Caperea with rorquals and grey whales, rather than right whales. This contrasts with traditional morphological classifications, but is in line with recent molecular evidence.
The finding of pygmy right whale fossils north of the equator is highly unexpected, and provides insights into ocean dynamics during the ‘age ages’. During cold periods associated with northern glaciation, equatorial waters cooled and allowed temperate and even subpolar species to cross the normally impermeable tropics. This process appears to have played a major, though until now underappreciated, role in shaping modern marine mammal distributions.
Our behavioural framework represent a major advance in classifying aquatic mammal feeding strategies, and demonstrates how entirely unrelated lineages have repeatedly followed similar evolutionary paths. It furthermore provides a novel hypothesis for the evolution of filter feeding in whales (suction first, filtering second) that is consistent with the fossil record. This is demonstrated by direct evidence of suction feeding in a variety of species, the presence of sharp teeth inconsistent with filtering, the apparent lack of baleen in archaic forms like Llanocetus, and a notable increase in mysticete body size that coincided with the loss of functional teeth.
Finally, our results trace the rise to dominance of filter feeders, and the gradual origin of mysticete gigantism. These insights are particularly relevant in light of the role of whales as ecosystem engineers, and thus their long-term effect on the evolution of the global marine ecosystem.
The finding of pygmy right whale fossils north of the equator is highly unexpected, and provides insights into ocean dynamics during the ‘age ages’. During cold periods associated with northern glaciation, equatorial waters cooled and allowed temperate and even subpolar species to cross the normally impermeable tropics. This process appears to have played a major, though until now underappreciated, role in shaping modern marine mammal distributions.
Our behavioural framework represent a major advance in classifying aquatic mammal feeding strategies, and demonstrates how entirely unrelated lineages have repeatedly followed similar evolutionary paths. It furthermore provides a novel hypothesis for the evolution of filter feeding in whales (suction first, filtering second) that is consistent with the fossil record. This is demonstrated by direct evidence of suction feeding in a variety of species, the presence of sharp teeth inconsistent with filtering, the apparent lack of baleen in archaic forms like Llanocetus, and a notable increase in mysticete body size that coincided with the loss of functional teeth.
Finally, our results trace the rise to dominance of filter feeders, and the gradual origin of mysticete gigantism. These insights are particularly relevant in light of the role of whales as ecosystem engineers, and thus their long-term effect on the evolution of the global marine ecosystem.