Behavioral Phenotyping of Naked Mole Rat (Heterocephalus glaber)

Transcription

1 Behavioral Bioassay IBRO Neuroscience School 2014 Behavioral Phenotyping of Naked Mole Rat (Heterocephalus glaber) Nilesh B. Patel Dept Medical Physiology University of Nairobi, Kenya

2 Richard Alexander In 1974 entomologist and evolutionary theorist Richard Alexander argued that "subsocial" behavior (that is parental care) and the opportunity for parental manipulation were even more powerful factors in the evolution of social behavior in insects (Alexander 1974). Across taxa, parental behavior correlates much more strongly with eusociality than does haplodiploidy (Andersson 1984; Alexander et al.1991). Alexander's critics argued that if parental care is a crucial precursor to eusociality, we should expect eusociality to have also evolved among the highly parental vertebrates: birds and mammals

3 His Response Alexander based an answer on his understanding of the selective forces involved in the evolution of insect eusociality and hypothesized a eusocial vertebrate.

4 Alexander predicted that a eusocial vertebrate's nest should be 1.Safe. 2.Expandable so that workers can enhance the value of the nest. 3.In or near an abundance of food that can be obtained with little risk. 4.Nest characteristics limitations suggested that the animal would be completely subterranean because few logs or trees are large enough to house large colonies of vertebrates. 5.Being subterranean further suggested that the eusocial vertebrate would be a mammal, even more specifically a rodent since many rodents nest underground. 6.The primary food of the hypothetical vertebrate would be large underground roots and tubers because the small grassy roots and grubs that moles feed on are so scattered that they are better exploited by lone individuals and would inhibit rather than encourage the evolution of eusociality. 7.The major predator of the hypothetical vertebrate would have to be able to enter the burrow but be deterred by the heroic acts of one or a few individuals. 8.The eusocial vertebrate was also expected to live in the wet-dry tropics because plants there are more likely to produce large roots and tubers that store water and nutrients to help them survive the dry periods. 9.The soil would need to be hard clay because otherwise the nest would not be safe from digging predators. 10.These two characteristics further suggested the open woodland or scrub of Africa.

5 He had no idea that a mammal with these characteristics existed. During lectures 1976 at Northern Arizona University at Flagstaff, mammalogist Terry Vaughan suggested to Alexander that his hypothetical eusocial rodent was a "perfect description" of the naked mole-rat Heterocephalus glaber. and suggested that Alexander contact Jennifer Jarvis, an authority on African mole-rats. Jarvis had studied the ecology and physiology of naked mole-rats but at that time nothing was known about their social system. Subsequent field and laboratory observations have confirmed that they are in fact eusocial, as Alexander's model had predicted, and that the other elements of his model are accurate as well (Braude and Lacey 1992; Jarvis 1981; Sherman et al 1991; 1992). This case demonstrates one type of predictive power in modern evolutionary theory.

6 Underground Burrows Underground Supermodels: What can a twentysomething naked mole-rat tell us about fighting pain, cancer, and aging? Thomas J. Park and Rochelle Buffenstein The Scientist June 1, 2012

7 Naked Mole Rat (Heterocephalus glaber) German naturalist Eduard Rüppell

8 Damarland Mole Rat

9 Interest in NMR Hypersensitivity to contact inhibition provides a clue to cancer resistance of naked mole-rat. Seluanova et al. PNAS (2009) 106 (46):19357 Genome sequencing reveals insights into physiology and longevity of the naked mole rat. Kim et al Nature (2011) 479:223. Amyloid beta and the longest-lived rodent: the naked mole-rat as a model for natural protection from Alzheimer's disease. Edrey et al. Neurobiol Aging. (2013) : S Blunted behavioral and c Fos responses to acidic fumes in the African naked mole-rat. LaVinka and Park. PLoS One. (2012)7(9):e Adult naked mole-rat brain retains the NMDA receptor subunit GluN2D associated with hypoxia tolerance in neonatal mammals. Peterson et al. Neurosci Lett. (2012) 506(2): A stereotaxic atlas of the brain of the naked mole-rat (Heterocephalus glaber). Xiao et al. Neuroscience. (2006) 141(3):

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11 Selective Inflammatory Pain Insenstivity in African Naked Mole-Rat (Heterocephalus glaber). Park et al PLoS Biology (2008) 6:e13. Lack substance P Acid insensitivity due Na v 1.7 variant which is inhibited by protons. St John Smith et al (2011) Science 334:1557

12 THE ANATOMICAL RECORD PART A 288A: (2006) Central Visual System of the Naked Mole-Rat (Heterocephalus glaber) SAMUEL D. CRISH, CHRISTINE M. DENGLER-CRISH, AND KENNETH C. CATANIA Superior colliculus and lateral geniculate nucleus severely atrophied. The olivary pretectal nucleus reduced but still retains its characteristic morphology, possibly indicating a role in light detection. Suprachiasmatic nucleus is well innervated and resembles the same structure in other rodents. The naked mole-rat appears to have selectively lost structures that mediate form vision while retaining structures needed for minimal entrainment of circadian rhythms. Light detection may still play an important role in the lives of these blind animals: most likely for circadian entrainment or setting seasonal rhythms.

13 The relative sizes of different sensory representations in naked mole-rats S1. Catania K C, and Remple M S PNAS 2002;99: by National Academy of Sciences

14 . Naked mole-rats: behavioural phenotyping and comparision with C57BL/6 mice. Deacon RM, Dulu TD, Patel NB. Behav Brain Res May 16;231(1): Species-typical Behaviors Motor Sensory Anxiety Cognition learning and memory

15 Species-Typical Behavior Test Parameter Mole-rats Mice (n=8) P (n=7,8) Burrowing Bedding 87.4 ± ± displaced (g) Food displaced (g) 9 ( ) ( ) Nesting Score 1.0 ( ) 2.5 ( ) Wt. untorn (g) 2.5 ( ) 1.3 ( ) Digging Latency (s) 36.3 ± ± No. bouts 8.9 ± ± 2.56 < Total digging 48.0 ± ± duration (s) Mean bout duration (s) 4.6 ( ) 1.7 ( ) Marble burying Marbles buried/ ( ) 9.0 ( ) Tunnel maze Tunnel entry 28.0 ( ( ) latency (s) 70.0) Tunnel entries 3.1 ± ± 0.80 < Time in 76.5 ( ( tunnels (s) 95.5) 121.0) Mean time/visit (s) 21.6 ( ) 11.2 ( )

16 GRAMS Nesting Score Species Typical Behavior Burrowing Food Pellets Digging NMR Mice NMR Mice NMR Mice Burrowing Bedding NMR MIce Latency No Bouts Nesting Total digging time NMR Mice NMR Mice

17 Motor Sensory Tests Test Parameter Mole-rats Mice P Open field Peripheral squares ± ± Central squares 6.6 ± ± Rears 3.0 ( ) 19.0 ( ) Holeboard Peripheral dips 0.0 ( ) 6.5 ( ) Central dips 0.0 ( ) 3.0 ( ) Rears 2.38 ± ± Test Parameter Mole-rats Mice P Inverted screen Time to fall (s) 0.0 ± ± 0.0 < Static rod Orient (s) 180 ( ) 7.0 ( ) < Transit (s) 180 ( ) 21.0 ( ) Pull-up test Pull-up time (s) 60.0 ( ) 1.0 ( ) <0.0001

18 Sensory Test Test Parameter Mole-rats Mice Schallert tape removal test Tape removal time (s) 420 ( ) 42.0 ( ) Honey test Latency to wipe face (s) 120 (26-120) 1.0 ( )

19 Second Olfaction Test Find the a 2 cm piece of banana buried in the bedding wood chips Olfaction 300 NMR Mice Sniff Dig Find

20 Light Dark Box Door size (cm) Parameter Mole-rats Mice 2 Latency (s) ± ± ± ± Dark time (s) 40.8 ± ± ± ± Transits 2.1 ± ± ± ± 2.04 Entry size dependent

21 Elevated Plus Maze Elevated Plus Maze NMR Mice 50 0 Open Entries Open Time Closed Entries Closed Time Central Time Parameter Mole-rats Mice Falls 4.0 ( ) 0.0 ( )

22 Cognitive Tests T-Maze Spontaneous Alternation Rewarded Alternation Cued Egocentric Position Discrimination

23 Summary A unique mammal. Surprisingly poor grip strength and motor sensory co-ordination. Not clearly concerned about being out in the open. Shows learning and memory Development of tests more suited to its evolutionary adaptation, physiology and habitat.

24 NMR Jokes