Got whiskers?

By Katie Pruett (Pitzer College) and Mari Purpura (Pitzer College) [Edited by Lars Schmitz, as part of BIOL 167 “Sensory Evolution”, an upper division class at the W.M. Keck Science Department. Written for educational purposes only].

The early evolution of mammals is accompanied by a number of important milestones, such as the evolution of a six-layered cortex and thermoregulation. Another distinguishing characteristic is the appearance of hair. Hair probably had a role in tactile sensing before it helped maintaining body temperature.

Some of the first hair may have been a form of whiskers. This would explain why so many terrestrial, as well as aquatic mammals have well developed mystacial (above lip) whiskers. Whiskers assist is exploratory behavior. Whisking is a form of active tactile sensing. In rodents, such as rats and mice, it is regulated by sensory feedback that boosts the sensory information available to animals (Mitchinson et al. 2007). This behavior has been observed in rodents and also in marsupials such as the gray short tailed opossum Monodelphis domestica.

Studying the gray short tailed opossum provides valuable insight into tracing the evolution of modern mammals. The presence of whisking in both rodents and marsupials presents the possibility that a common ancestor to all modern marsupials and placental animals may have used active vibrissal sensing or whisking (Grant et al. 2013). The vibrissal musculature of the rat has been described in detail, but that of the opossum had not been thoroughly described prior to the publication of this paper (Haidarliu 2010, 2012; Robyn et al. 2013). This paper has contributed a great deal of exciting detail on whisker musculature and anatomy of the possum, as well as the evolutionary emergence of whiskers in a common ancestor of both marsupials and rodents.

Figure 1. The model organism, opossum (Monodelphis domestica) whose mystacial whisker pad was studied in order to compare the evolutionary relationship in vibrissal sensing between rodents and marsupials. [By Dawson at en.wikipedia [CC-BY-SA-2.5 (http://creativecommons.org/licenses/by-sa/2.5)], from Wikimedia Commons http://commons.wikimedia.org/wiki/File:Monodelphis_domestica.jpg].

Figure 1. The model organism, opossum (Monodelphis domestica) whose mystacial whisker pad was studied in order to compare the evolutionary relationship in vibrissal sensing between rodents and marsupials. [By Dawson at en.wikipedia [CC-BY-SA-2.5 (http://creativecommons.org/licenses/by-sa/2.5)], from Wikimedia Commons
http://commons.wikimedia.org/wiki/File:Monodelphis_domestica.jpg].

Grant et al. aimed to investigate whether active vibrissal sensing was present in ancestral mammals or whether whisking behavior amongst marsupials and placental animals was a result of convergent evolution. The hypothesis of convergent evolution for active vibrissal sensing in both rodents and marsupials would appear much less likely with evidence that the underlying mechanisms, and not just the physical appearance, are similar.

Grant’s group examined similarities and discrepancies observed between the opossums and rats in order to draw conclusions about when whiskers evolved in the evolutionary history. Here’s what they did in detail (jump to the next paragraph if you want to skip the methods). They looked at the whisker and mystacial pad anatomy of the gray short tail opossum, Monodelphis domestica, using four animals, from which they dissected and the preserved the mystacial pads. They were able to make direct comparisons between the whisker layout and vibrissal musculature of the opossum and that of the common rodent using digital microscopy. They replicated the methodology of earlier studies of the rat facial musculature using cytochrome oxidase (CCO) staining to obtain digital microscope images of the opossum mystacial pad (Haidarliu et al. 2010). This methodological replication also helped investigate whether the opossum’s large facial whiskers are moved by an intrinsic sling-like musculature that connects each whisker to the adjacent one among each whisker row. Active whisking was observed in 26 live opossums. Filming and behavioral studies took place in a custom-built light box under infrared light and compared it to video footage of rats under similar conditions.

Grant et al. found that opossums have fewer whiskers than rats, however the vibrissal musculature is similar. Both have intrinsic and extrinsic muscles with the intrinsic muscles positioned as slings linking pairs of large vibrissae within rows. And both “whisk” actively!

In comparing the vibrissal musculature of the opossum and common rodent, both were shown to employ similar underlying mechanisms. This finding is concurrent with earlier results that have suggested similar patterns of vibrissal musculature (Haidarliu et al. 2010). The opossum mystacial pad has a grid like follicle layout, with nasal and maxillary compartments. There are fewer whisker rows than in rats, however in both species the whiskers are coupled together within rows by horizontal intrinsic muscles. The superficial extrinsic muscles were generally similar to those in rats but the deep retracting and extrinsic muscles appeared to be considerably less developed in the opossum. This contributes to the overall appearance of the mystacial pad as less substantial in the opossum compared to the rat.

Figure 2. Opossum whiskers (left) compared to rat whiskers (right). Both species have whiskers arranged in a similar grid-like pattern, however the opossum has only 23 compared to 30 in most rodents. In the opossum, the whiskers form four rows (c), whereas the rat has five rows (d). The two species have some whiskers that differ in location and type, but overall the organization and underlying musculature is similar (e and f). Overall, the mystacial pad is less prominent in the opossum compared to the rat from both the side and top angles (a and b, g and h),  but structurally opossum whiskers  have many similarities to the vibrissal follicles of the rat. [Figure 1 of Grant et al. 2013].

Figure 2. Opossum whiskers (left) compared to rat whiskers (right). Both species have whiskers arranged in a similar grid-like pattern, however the opossum has only 23 compared to 30 in most rodents. In the opossum, the whiskers form four rows (c), whereas the rat has five rows (d). The two species have some whiskers that differ in location and type, but overall the organization and underlying musculature is similar (e and f). Overall, the mystacial pad is less prominent in the opossum compared to the rat from both the side and top angles (a and b, g and h), but structurally opossum whiskers have many similarities to the vibrissal follicles of the rat. [Figure 1 of Grant et al. 2013].

Some of these differences in mystacial musculature are likely to relate to qualitative differences in the capacity of the animal to control their whiskers during active sensing behaviors. Analyses of rat whisking during exploration of objects have shown that these animals have the capacity to reduce the angular spread of their whiskers in a manner that increases whisker tip contact with surfaces of interest. As shown in earlier studies, there appears to be a common ancestor to all modern marsupials and placental mammals that may have employed active vibrissal sensing.

The current study provides compelling evidence that whisking in rodents and marsupials uses similar underlying mechanisms and is therefore unlikely to be convergent, but rather a homologous trait.

Figure 3. The evolutionary relationship between opossums and rats. The research suggests that the common ancestor must have had an active vibrissal sensing system.  [Edited. Original image by Fred Hsu (Wikipedia:User:Fredhsu on en.wikipedia) (Image generated and uploaded by user) [GFDL (http://www.gnu.org/copyleft/fdl.html) or CC-BY-SA-3.0 (http://creativecommons.org/licenses/by-sa/3.0/)], via Wikimedia Commons.  http://commons.wikimedia.org/wiki/File:The_Ancestors_Tale_Mammals_cladogram.png].

Figure 3. The evolutionary relationship between opossums and rats. The research suggests that the common ancestor must have had an active vibrissal sensing system.
[Edited. Original image by Fred Hsu (Wikipedia:User:Fredhsu on en.wikipedia) (Image generated and uploaded by user) [GFDL (http://www.gnu.org/copyleft/fdl.html) or CC-BY-SA-3.0 (http://creativecommons.org/licenses/by-sa/3.0/)], via Wikimedia Commons.
http://commons.wikimedia.org/wiki/File:The_Ancestors_Tale_Mammals_cladogram.png].

The gray short tailed opossum engages in active vibrissal sensing behaviors that have also been described in mice and rats. Authors found that the mystacial muscle system of the opossum is very similar to that of rodent whisker specialist containing four key muscle groups (intrinsic, superficial extrinsic, the deep retracing and the extrinsic protracting muscles). These results suggest that the intriguing possibility that active vibrissal sensing may therefore have been a key driver for the evolution of cortical motor control in early mammals. Interestingly the opossum cortex lacks a distinct motor area, and the only area of the body in which movement can be elicited by direct cortical microstimulation is the vibrissal region around the snout (Frost et al. 2000). If early mammals actively moved their vibrissae then this has important implications for many other aspects of mammalian evolution.

This research presented by Grant et al. builds upon and confirms previous work in the field of mammalian evolution. Recent studies described the vibrissal musculature and whisking movement of rats (Haidarliu, 2010, 2012). In fact, Grant et al. replicated the methodology used in those studies to study opossums. Grant already was a co-author of an earlier work in which they studied the ‘whisking’ behavior of rats, mice, and opossums and how it is controlled in relation to their bodies and the structures in the environment (Mitchinson et al. 2011). Grant et al.’s current work is largely a follow-up study to Mitchinson’s 2011 work. This paper is the first that specifically focuses on the evidence from vibrissal musculature and function that aims to determine the evolutionary relationship between marsupials and rodents, and thus does not contradict previous results. Perhaps later studies will contradict the findings presented here or further support them.

A study that could advance the field in the future would be to study the innervation of the whiskers in the both opossums and rats. Grant et al. focused on the overall similarity in appearance and musculature of the mystacial pads of opossums and rats, but did not study whether or not the nerve fibers that connect the whiskers to the brain are also similar. If the genome of opossums and rats are sequenced, they could attempt to determine which genes are responsible for the mystacial pad and whiskers and determine whether there is any sequence homology between the two species. Finding similarities in the nerve morphology as well as in the genetic sequence would provide further convincing evidence that vibrissal sensing in the two species is indeed a result of a common ancestor with this ability. The fossil record has not been a useful tool in researching this topic so far, as no fossils have been found that have well-preserved traces of facial musculature (Ji et al. 2002; Luo, 2007; Luo et al. 2011). Perhaps one day, useful fossils will be discovered or advanced techniques of fossil reconstruction will make it possible to analyze those that we already have.

There is a lot of work that still needs to be done in the field, but these novel findings by Grant et al. are a big step in the right direction!

References

Frost, SB, Milliken, GW, Plautz, EJ, Masterton, RB and Nudo, RJ. (2000). Somatosensory and motor representations in cerebral cortex of a primitive mammal (Monodelphis domestica): a window into the early evolution of sensorimotor cortex. Journal of Comparative Neurology 421: 29-51. (DOI: 10.1002/(SICI)1096-9861(20000522)421:1<29::AID-CNE3>3.0.CO;2-9).

Grant RA, Haidarliu S, Kennerley NJ, Prescott TJ. (2013). The evolution of active vibrissal sensing in mammals: evidence from vibrissal musculature and function in the marsupial opossum Monodelphis domestica. The Journal of Experimental Biology 216: 3483-3494. (DOI: 10.1242/ jeb.087452)

Haidarliu S, Simony E, Golomg D, Ahissar E. 2010 Muscle architecture in the mystacial pad of the rat. The Anatomical Record 293(7): 1192-1206. (DOI: 10.1002/ar.21156)

Haidarliu S, Golomg D, Kleinfeld D, Ahissar E. 2012 Dorsorostral snout muscles in the rat subserve coordinated movement for whisking and sniffing. The Anatomical Record 295(7): 1181-1191. (DOI: 10.1002/ar.22501)

Ji, Q, Luo ZX., Yuan CX, Wible, JR, Zhang, JP and Georgi JA (2002). The earliest known eutherian mammal. Nature 416: 816-822. (DOI: 10.1038/416816a)

Luo, Z. X. (2007). Transformation and diversification in early mammal evolution. Nature 450: 1011-1019. (DOI: 10.1038/nature06277)

Luo, Z. X., Yuan, C. X., Meng, Q. J. and Ji, Q. (2011). A Jurassic eutherian mammal and divergence of marsupials and placentals. Nature 476: 442-445. (DOI: 10.1038/nature10291)

Mitchinson B, Grant RA, Arkley K, Rankov V, Perkon I, Prescott TJ. 2011 Active vibrissal sensing in rodents and marsupials. Philosophical Transactions of the Royal Society London B 366 (1581), 3037-3048. (DOI: 10.10.1098/rstb.2011.0156)

Robyn GA, Haidarliu S, Kennerley NJ, Prescott TJ. 2013 The evolution of active vibrissal sensing in mammals: evidence from vibrissal musculature and function in the marsupial opossum Monodelphis domesticus. Journal of Experimental Biology 216, 3483-3494. (DOI 10.1242/jeb.087452)

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