Periodic Reporting for period 1 - Evo-Devo-Whales (From Land to Water: the Role of Development in the Evolution and Diversification of Baleen and Toothed Whales)
Période du rapport: 2020-09-07 au 2022-09-06
Cetaceans (baleen whales and toothed whales) are a distinctive group of mammals that has evolved unique adaptations to live in water. Their impressive fossil record traces their evolution from their terrestrial ancestors (Artiodactyla) to the present aquatic forms. All living cetaceans have flippers instead of limbs, possess a blowhole at the top of the head instead of an anteriorly positioned nose. They have also developed a characteristic head shape connected to their feeding mode: while baleen whales have lost their teeth and feed using keratinous plates called baleen, toothed whales have evolved the ability to locate their prey using sound waves (echolocation). Changes in prenatal development (ontogeny) played a major role in allowing these animals to evolve the skull adaptions they currently display related to their peculiar traits. Though, little information is available on their development, limiting our understanding of the role of ontogeny in the evolution of modern cetaceans. A better understanding of Cetacea life history can help inform conservation policies.
This project applied 3-dimensional (3D) imaging and cutting-edge geometric morphometric (GM) and phylogenetic methods to quantify the development of skull shape in a diverse sample of cetaceans in order to reconstruct how development has shaped the evolution and diversification of this unique group of mammals. I produced high-quality 3D datasets that will be shared in on-line repositories, making rare fetal specimens of toothed and baleen whales accessible for further research and for outreach initiatives and preserving them for future generations.
Specifically, I addressed the following questions: 1) How does skull prenatal development vary across toothed whales? Here, I focused on the changes in skull asymmetry, a peculiar trait of toothed whales, during ontogeny and how these differences influence the ecological and hearing adaptations in different species. 2) How does ear bones development differs between low-frequency hearing baleen whales and high-frequency hearing toothed whales? Here I used innovative methods to quantify changes in shape without the use of landmarks to study the differences in ossification and ontogeny in two major ear bones, the tympanic bulla and the periotic, in the two group of Cetacea, connecting them to the evolution of their disparate hearing adaptations. 3) How does skull development vary between toothed and baleen whales? Here I focused on changes in the rostrum and braincase during the ontogeny of the two groups to understand how ontogeny has influenced the evolution of their unique feeding adaptations and has helped them adapt to life in water.
We collected 3D data and built a dataset comprised of over 200 specimens of Cetacea at all stages of development, from embryos to adult, and spanning the diversity of the group. Using this impressive dataset and novel GM, statistical and phylogenetic comparative methods we were able to answer our main research questions. 1) We found that skull asymmetry progressively increases during ontogeny, and the level of asymmetry at the early fetal stages as well as the distribution of asymmetry in the adults is directly correlated with the evolutionary history of the species, while the high or low levels of asymmetry displayed in the adults are directly correlated with the ecology and hearing adaptations of the species. 2) Examining ear bone development, we found significant differences in ossification sequence and shape ontogeny in the periotic bone between the two groups, baleen and toothed whales, but not in the tympanic bulla. This is directly related to both their common ancestry and adaptations for underwater hearing, reflected in the tympanic bulla, and their different hearing frequencies, which depend on the internal morphology of the periotic bone. 3) We are currently finishing examining the relationship between changes in skull ontogeny and evolution of different feeding adaptations across this group. Generally, we see convergent but not shared ontogenetic patterns in braincase development between baleen and toothed whales, reflecting their convergent evolution towards a telescoped cranium, where the bones overlap and the nasals are retracted towards the back of the skull. The rostrum ontogeny is more disparate, reflecting major ecological differences particularly among toothed whales.
This project applied 3-dimensional (3D) imaging and cutting-edge geometric morphometric (GM) and phylogenetic methods to quantify the development of skull shape in a diverse sample of cetaceans in order to reconstruct how development has shaped the evolution and diversification of this unique group of mammals. I produced high-quality 3D datasets that will be shared in on-line repositories, making rare fetal specimens of toothed and baleen whales accessible for further research and for outreach initiatives and preserving them for future generations.
Specifically, I addressed the following questions: 1) How does skull prenatal development vary across toothed whales? Here, I focused on the changes in skull asymmetry, a peculiar trait of toothed whales, during ontogeny and how these differences influence the ecological and hearing adaptations in different species. 2) How does ear bones development differs between low-frequency hearing baleen whales and high-frequency hearing toothed whales? Here I used innovative methods to quantify changes in shape without the use of landmarks to study the differences in ossification and ontogeny in two major ear bones, the tympanic bulla and the periotic, in the two group of Cetacea, connecting them to the evolution of their disparate hearing adaptations. 3) How does skull development vary between toothed and baleen whales? Here I focused on changes in the rostrum and braincase during the ontogeny of the two groups to understand how ontogeny has influenced the evolution of their unique feeding adaptations and has helped them adapt to life in water.
We collected 3D data and built a dataset comprised of over 200 specimens of Cetacea at all stages of development, from embryos to adult, and spanning the diversity of the group. Using this impressive dataset and novel GM, statistical and phylogenetic comparative methods we were able to answer our main research questions. 1) We found that skull asymmetry progressively increases during ontogeny, and the level of asymmetry at the early fetal stages as well as the distribution of asymmetry in the adults is directly correlated with the evolutionary history of the species, while the high or low levels of asymmetry displayed in the adults are directly correlated with the ecology and hearing adaptations of the species. 2) Examining ear bone development, we found significant differences in ossification sequence and shape ontogeny in the periotic bone between the two groups, baleen and toothed whales, but not in the tympanic bulla. This is directly related to both their common ancestry and adaptations for underwater hearing, reflected in the tympanic bulla, and their different hearing frequencies, which depend on the internal morphology of the periotic bone. 3) We are currently finishing examining the relationship between changes in skull ontogeny and evolution of different feeding adaptations across this group. Generally, we see convergent but not shared ontogenetic patterns in braincase development between baleen and toothed whales, reflecting their convergent evolution towards a telescoped cranium, where the bones overlap and the nasals are retracted towards the back of the skull. The rostrum ontogeny is more disparate, reflecting major ecological differences particularly among toothed whales.
I have collected data from the extensive collections of the Natural History Museum using non-destructive computed tomography (CT) and surface scanning techniques. I then adapted and applied cutting-edge quantitative geometric morphometrics (GM) methods and a variety of statistical analyses in R, including Bayesian phylogenetic methods, to characterize and compare the changes in morphology during development among families of toothed whales with different feeding adaptions as well as between toothed and baleen whales.
I published two peer-reviewed articles stemming from this project, and two more are currently being prepared. I presented parts of this project SICB +, SVP and Society of Marine Mammalogy international meetings. I also disseminated the results of this project to different schools in Italy during ‘Science is Wonderful!’ 2021. Disruption caused by Covid-19 did not allow me to fulfill one of the original objectives, investigating differences in skull development between Cetacea and their closely related terrestrial relatives even-toed ungulates. I will explore this question in future research projects and by collaborating with colleagues at the NHM.
I published two peer-reviewed articles stemming from this project, and two more are currently being prepared. I presented parts of this project SICB +, SVP and Society of Marine Mammalogy international meetings. I also disseminated the results of this project to different schools in Italy during ‘Science is Wonderful!’ 2021. Disruption caused by Covid-19 did not allow me to fulfill one of the original objectives, investigating differences in skull development between Cetacea and their closely related terrestrial relatives even-toed ungulates. I will explore this question in future research projects and by collaborating with colleagues at the NHM.
This project investigated the relationship between ontogeny and evolution in Cetacea, baleen and toothed whales. Using an integrative approach combining state-of-the-art digitization and phenomic methods and phylogenetic comparative analyses, I was able to show that skull ontogeny is directly responsible for the development of skull asymmetry in toothed whales. I have also demonstrated how ear bone development reflects both the shared ancestry of the two cetacean groups as well as their different hearing frequency adaptations: the tympanic bulla preserves a common ontogeny while the periotic development is significantly different between the two groups. Skull development also reflects the ecological and feeding differences in baleen and toothed whales, with the latter groups presenting a more diverse ontogeny in light of their more varied feeding adaptations. These results are novel and open up new areas of research on how development may be fostering biodiversity. This is particularly important in the face of the sixth mass extinction where one-fifth of all living species are threatened. It is indeed crucial to identify what changes in ontogeny are connected to different ecological adaptations. In the future, I will explore how development has played a role in the evolution of Cetacea aquatic adaptations, helping deepen our understanding of the evolution and potential for adaptation of this group. Additionally, the specimens digitized for this project will allow other researcher to study other aspects of development in Cetacea, such as limb or brain ontogeny. They will also be used in outreach activities and public interactive exhibits to help inform the public on the life history of baleen and toothed whales and the importance of museum collections in conservation research.