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Evolution of the Cochlea and Hearing in Odontocetes

Periodic Reporting for period 1 - ECHO (Evolution of the Cochlea and Hearing in Odontocetes)

Reporting period: 2017-10-02 to 2019-10-01

Knowledge of cetacean hearing has increased in recent years, but still remains biased towards physiological experiments, often on a single species, such as the common bottlenose dolphin. Now, the greatest knowledge gap concerns the acoustic mechanisms of the cochlea, the organ that has the pivotal role of converting sound waves into nerve signals. Studies of cetacean cochlea have not yet progressed beyond qualitative descriptions, which are valuable from a comparative point of view, but add little to our understanding of what frequencies can actually be detected. Hearing abilities are intricately linked to detailed cochlear shape, which can only be determined using quantitative techniques. It is therefore imperative that quantitative shape analyses of the cochlea be undertaken to enable us to truly understand cetacean hearing and its evolution. ECHO has investigated how and when odontocetes evolved their unique sensory abilities, by integrating state-of-the-art 3D imaging, shape quantification and statistical analyses and applying them, for the first time, to the cochlea.

The sensitivity of cetacean hearing has rendered them particularly vulnerable to anthropogenic noise pollution, therefore gaining a better understanding of the different sounds these animals are hearing will be important for society and more specifically, inform future conservation and management policies on the effect of this phenomenon.

The research objectives of ECHO are as follows:
1. To explore the diversity of the cochlea in living odontocetes.
2. To identify when odontocetes began to use echolocation.
3. To test the extent to which “river dolphins” display convergent evolution in their cochlea.
Work Package 1: To explore the diversity of the cochlea in living odontocetes.
We microCT scanned over 50 species of modern odontocete periotics (the bone containing the cochlea) at NHM IAC as well as several other international institutions. After creating the 3D cochlear models from the raw data and then landmarking them, we then performed geometric morphometric analyses on this dataset to quantify differences between species. We then compiled a dataset of ecomorphological variables to perform a series of Chi-squared tests to test for correlations between them1.
This work significantly advances the state-of-the-art as it more than doubles the number of odontocete taxa for which there are cochlear models. It also has provided the first detailed tests of which variables are correlated with cochlear shape, informing future potential macroevolutionary hypotheses about odontocetes more broadly.

Work Package 2: Identify when odontocetes began to use echolocation.
We microCT scanned over 20 species of fossil odontocete periotics at NHM IAC as well as several other international institutions. Cochlear models from these scans have also been made and landmarked. These data have been combined with the dataset of work package 1 and shape differences have been quantified. These data are currently being used in analyses tracking how cochlear shape of odontocetes has changed over time and when the shape associated with being able to echolocate first evolved (in progress), as well as more focused paper on cochlear evolution of platanistoids (represented today by the ganges river dolphin, but in the past the group was much more diverse), in collaboration with colleagues in Argentina and New Zealand.
Additionally, a paper on an exceptionally preserved new species of fossil toothed whale is also in progress. The fossil was prepared using acid preparation techniques, ensuring that its excellent preservation has been retained. It also preserves its earbones allowing critical new data on the hearing abilities of early toothed whales to be obtained. Preliminary results indicate this individual may have not been able to echolocate, differing from all living odontocetes and showing a new intermediate stage in odontocete evolution. However, some of these results were also reached independently by a separate research group and published in 20194, meaning that our paper has had to be refocused, delaying progress.

Work Package 3: To test the extent to which “river dolphins” display convergent evolution in their cochlea.
This work package was expanded from its original scope looking at river dolphins only to looking at all modern odontocetes. We took the dataset created in work package 1 and used it for this work package. We ran a series of analyses that: 1) determined if convergent evolution had occurred in any toothed whale lineages 2) tested to see if this convergence was statistically significant and 3) tested for correlations between these convergent lineages and a range of ecomorphological variables. We also found that the two deepest diving groups of toothed whales, the beaked whales and sperm whales, have convergently evolved a similar shaped cochlea. We believe this is due the strong selection pressures exerted by the extreme acoustic environment at the depths these animals are diving to. This paper was published in 2019 in collaboration with researchers from England, Switzerland and France.
This project has and will continue to advance our knowledge of hearing in toothed whales, as well as the field of sensory biology more broadly. More personally, I have benefited enormously from being based at the NHM during my fellowship. I have gained a large amount of new technical expertise, particularly in phylogenetic comparative methods and the use of the R programming language. This has primarily come from my host, Dr Natalie Cooper, who has been tremendously supportive and helpful. We have also co-supervised a Masters student together, giving vital experience as a supervisor and mentor. The broader research environment and collection at the NHM has also been very intellectually stimulating, resulting in two additional publications5,6 on top of the one arising directly from my fellowship research, as well as three further papers that are currently in peer review. This research effort, the professional network, and the new skill set I have acquired over the last two years have greatly strengthened my research profile. This is demonstrated by my successfully being awarded a one year Postdoctoral Research Assistant position (under ERC Starting Grant 677774 (TEMPO)) at the University of Oxford which I commenced directly after completing my fellowship at the NHM.

The results of this project have been communicated via talks at the 62nd Palaeontological Association Annual Meeting (Bristol, UK, 2018) and 5th International Palaeontological Congress (Paris, France, 2018), as well as an invited symposium talk at the 12th Triennial Congress of the International Society of Vertebrate Morphologists (Prague, Czech Republic, 2019). The research has been further disseminated via public talks on cetacean evolution at the NHM (including the annual European Researchers Night) and the University of Cambridge, as well as on social media (Twitter). Wherever possible, EU funding was acknowledged as part of these activities.

In total, to date the research efforts of this project have resulted in 3 publications1,5,6 as well as three more currently in peer review. All papers have been published in Open Access journals and the data has either been made available as supplementary material or put on the NHM Data Portal. All publications contain a reference to EU funding, specifying the grant identifier and acronym.