Symposium IV: Murinae as a Model System 16:00 - 18:00 Monday, 1st July, 2019 Location Regency BCD Session Type Murinae as a Model System Event Type Symposium

4:00 - 4:05 PM

Welcome & Introduction (Jacob A. Esselstyn) Description - The Murinae comprises over 11% of mammalian species, and includes the two most important mammalian model species for genomic and biomedical research (lab mouse and rat), as well as some of the most ecologically and economically destructive invasive species (black rat and Norwegian rat). However, murines are much more than their famous model and invasive species suggest to the public and many biologists. In addition, to their taxonomic diversity, the Murinae spans an incredible breadth of ecological and phenotypic diversity representing a wide range of diets (omnivores, vermivores, folivores, etc.), locomotory modes (arboreal to semi-aquatic), reproductive strategies (r- and k-selected), body sizes (three orders of magnitude), pathogen loads, and many other dimensions. This incredible ecological diversity evolved rapidly over the last 14 million years as the group spread across the Old World. Much of this diversity (~70%) resides in the Indo- Australian region and arose through a process of repeated colonization of islands and subsequent diversification. This history of replicated radiations provides a natural experiment for understanding how lineages, genomes, and phenotypes diversify in an ecological context. Organizers: Jake Esselstyn and Kevin Rowe.

16:05 - 16:28

217 Systematics of Murinae and biogeography of an adaptive radiation

Kevin C Rowe1,2, Emily J Roycroft1,2, Pierre-Henri Fabre3, Jonathan A. Nations4, Jacob A. Esselstyn4 1Museums Victoria, Melbourne, VIC, Australia. 2University of Melbourne, Melbourne, VIC, Australia. 3Universite Montpellier, Montpellier, Occitanie, France. 4Louisiana State University, Baton Rouge, LA, USA

Abstract Body

Representing >10% of living mammals, the more than 700 species of murines (Old World rats and mice) arose over the last ~14 million years. The two most powerful mammalian model organisms (lab mouse and rat) emerged from this radiation, however, much of murine diversity remains unexplored. Since their origin, the Murinae repeatedly colonized Eurasia, Africa, and Indo-Australia with at least ten transitions across Wallace’s line to reach Sulawesi, the Philippines and Sahul (Australia and New Guinea). Following these transitions, murine rodents adapted to a wide range of environments and ecomorphological niches. This history of repeated colonization and replicated radiations in murines provides an ideal scenario for testing the role of ecological selection in shaping diversification. For instance, on Sulawesi and the Philippines, shrew rats and their relatives, have evolved convergently extreme phenotypes through rapid rates of morphological evolution. In Australia, transitions between arid and mesic biomes occurred repeatedly in the phylogenetically-nested genus Pseudomys. We will provide a review of murine diversity and their bieogeographic history with emphasis on their repeated radiations across the Indo-Australian Archipelago. Our systematic framework provides the foundation for pushing murines from a two-species genomic model to a 700-species adaptive radiation model with unusually rich genomic and phenotypic resources. 16:28 - 16:51

218 Convergences in the jaw muscle system among the independently derived worm-eating specialist murines

Pierre-Henri Fabre1, Lionel Hautier2, Anthony Herrel3, Lawrence Heaney4, Kevin Rowe5, Anang Achmadi6, Jacob Esselstyn7 1UM, ISEM, Montpellier, Hérault, France. 2CNRS, ISEM, Montpellier, Hérault, France. 3CNRS, MNHN, Paris, Paris, France. 4Field Museum, Chicago, Illinois, USA. 5Melbourne Museum, Melbourne, Victoria, Australia. 6MZB, Bogor, Bogor, Indonesia. 7LSU, Baton Rouge, Louisianna, USA

Abstract Body

Spectacular ecomorphological shifts are often associated with historical events that presumably opened ecological opportunities. One of the most spectacular ecomorphological changes is the repeated shift from omnivory to vermivory among Indo-Pacific rodents. Worm-eating murines are morphogically very distinctive, which led early taxonomists to group several genera in their own subfamily, the Rhynchomyinae. However, recent phylogenetic studies have demonstrated that these anomalous murines are convergently derived. We combined classical and contrast enhanced dissections to study the craniomandibular system of these unusual insular rodents. The dietary shift to vermivory involved major morphological changes of the cranio-mandibular system including elongated rostrum and jaw, loss or reduction of cheek teeth, a highly mobile jaw symphysis, and modifications of the alisphenoid region of the skull. A major reshaping of the mammalian cranio- mandibular muscle system also occurred with the reduction of the masseteric region indicating a loss of gnawing and chewing capacities. Notably, we found that these rodents have extremely large pterygoid muscles associated with high capacity for forward-back and medio-lateral jaw movements. These morphological changes likely allow these worm-eating rats to use their jaw like a precision tool to manipulate and ingest earthworms largely without chewing. The repeated origin of this suite of traits suggests that ecological opportunity is strong and/or potential developmental pathways are shared by murines that have been evolving independently for the last ~8 million years.

Did an ASM award and/or grant assist in your research that culminated in this submission?

NSF DEB-1754096 16:51 - 17:14

219 Adaptive evolution during the diversification of murine rodents revealed by whole exomes

Emily J Roycroft1,2, Anang Achmadi3, Jacob A Esselstyn4,5, Jeffrey M Good6, Adnan Moussalli2,1, Kevin C Rowe2,1 1School of BioSciences, The University of Melbourne, Melbourne, Victoria, Australia. 2Museums Victoria, Melbourne, Victoria, Australia. 3Museum Zoologicum Bogoriense, Research Center for Biology, Cibinong, Jawa Barat, Indonesia. 4Museum of Natural Science, Louisiana State University, Baton Rouge, Louisiana, USA. 5Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana, USA. 6Division of Biological Sciences, University of Montana, Missoula, Montana, USA

Abstract Body

Species that colonize novel environments are faced with unfamiliar assemblages of biotic and abiotic factors, to which they must adapt in order to survive. Changes in selective pressures during this process are expected to be measurable at the genomic level. Screening for differences in signatures of selection across genes and species, and how these associate with predicted gene function, can provide insight into the genetic basis of adaptive evolution. The rodent subfamily Murinae comprise greater than 11% of all mammal species, a diversity which has accumulated both recently and rapidly as they spread across the Old World. Murines are adept colonizers, and their diversification is typified by repeated colonization of new landmasses, islands and environments, especially in the Indo-Australian region. To examine the evolution of protein-coding genes during the colonization and diversification process, we sequenced whole-exomes from 47 species of murine rodents, primarily spanning the Indo-Australian Archipelago. Using a radiation-wide approach to detecting positive selection, we find genes associated with adaptation to novel environments, especially those that are likely involved in an evolutionary “arms-race” with pathogens, have been subject to pervasive diversifying selection. We additionally identify accelerated evolution in genes associated with lactation and bitter taste. Our results highlight both categories of genes, and specific genes, which may have played an integral role in the success of murine rodents in novel environments and ecological contexts.

Did an ASM award and/or grant assist in your research that culminated in this submission?

This research was supported by an ASM Grant-in-Aid of Research awarded to Emily Roycroft in 2017 17:14 - 17:37

220 The developmental basis of pigment pattern evolution in rodents

Ricardo Mallarino Princeton University, Princeton, NJ, USA

Abstract Body

Mammalian color patterns are among the most conspicuous characters found in nature and can have a profound impact on fitness. However, little is known about the mechanisms underlying their formation and subsequent evolution. We capitalized on the naturally occurring color pattern of the African striped mouse, Rhabdomys pumilio, to investigate the formation of periodic stripes, a common pattern in mammals. In striped mice, stripes result from underlying differences in melanocyte maturation, which give rise to spatial variation in hair color. Through transcriptomic analyses of the developing skin, we identified the transcription factor Alx3 as a major hierarchical regulator. During striped mouse embryogenesis, patterned expression of Alx3 precedes pigment stripes and acts to directly repress Mitf, a master regulator of melanocyte differentiation. Moreover, Alx3 is also differentially expressed in the dorsal stripes of chipmunks, which have independently evolved a similar color pattern. Thus, differences in the spatial control of Alx3 lead to striped patterns in rodents, revealing both a new factor regulating pigment cells and a previously unappreciated mechanism for modulating hair color. I’ll end by discussing how my lab, through a variety of multidisciplinary approaches, uses stripe pattern formation as a model to uncover molecular mechanisms underlying the origin of evolutionary innovations. 17:37 - 18:00

221 Rats get dirty in the city: The impact of urbanization on rodents and rodent-borne diseases

Cadhla Firth James Cook University, Cairns, QLD, Australia

Abstract Body

Urbanization is a global phenomenon that has led to a rapid increase in both the number of people living in cities and the proportion of land mass occupied by urban environments. Although the process of urbanization destroys and fragments natural habitats, it also creates new ecological niches and provides access to abundant resources, allowing some species to thrive. Rodents are among the most successful urban mammals, with several species distributed globally in cities (e.g., members of the genera Mus and Rattus), and many others persisting locally in urban and suburban areas. However, unlike many other species of urban wildlife, rodents often live closely with people and come into contact with many aspects of our food supply. As a result, people are often at risk from the pathogens carried by rodents. Our work seeks to understand how the ecological and environmental context of cities shapes the abundance and distribution of urban rodents and the pathogens they carry. Here, we explore how features of the urban environment influence human disease risk, and discuss how a One Health-based approach to urban rodent management can be used to ensure the continued and healthy coexistence of people and rodents in city environments.

Did an ASM award and/or grant assist in your research that culminated in this submission?

No