Cuthill, Innes C

Innes C. Cuthill

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Nature Plants

Flower colour: Gloger's rule isn't just for the birds

A 180-year-old ‘law’ in zoology has found its best support so far in a study of floral colour, which not only documents darker plants growing closer to the equator, but also supports the idea that the colour stems from ultraviolet protection

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                          Cuthill, I. C. (2015). Flower colour: Gloger's rule isn't just for the birds.Nature Plants, 1, [14013]. 10.1038/nplants.2014.13Peer reviewed versionLink to published version (if available):10.1038/nplants.2014.13Link to publication record in Explore Bristol ResearchPDF-documentUniversity of Bristol - Explore Bristol ResearchGeneral rightsThis document is made available in accordance with publisher policies. Please cite only the publishedversion using the reference above. Full terms of use are available:http://www.bristol.ac.uk/pure/about/ebr-terms.htmlTake down policyExplore Bristol Research is a digital archive and the intention is that deposited content should not beremoved. However, if you believe that this version of the work breaches copyright law please contactopen-access@bristol.ac.uk and include the following information in your message:• Your contact details• Bibliographic details for the item, including a URL• An outline of the nature of the complaintOn receipt of your message the Open Access Team will immediately investigate your claim, make aninitial judgement of the validity of the claim and, where appropriate, withdraw the item in questionfrom public view.1  [Ontology terms] Biological sciences / Plant sciences / Plant reproduction / Flowering Biological sciences / Plant sciences / Natural variation in plants Biological sciences / Evolution Biological sciences / Plant sciences / Plant evolution  Flower colour: Gloger’s Rule isn’t just for the Birds  Innes C. Cuthill  A 180 year-old “law” in zoology has found its best support to date in a study of floral colour. This not only documents darker plants growing closer to the equator but also supports the idea that it all stems from ultraviolet protection.    As long ago as 1833 the German ornithologist Constantin Lambert Gloger noted that birds from warmer regions (usually interpreted as the tropics) tend to be darker than related species from cooler areas1. Since then “Gloger’s Rule” has been observed in several bird and mammal species as well as humans. In this issue Koski and Ashman breathe new life into this old idea by investigating the phenomenon in plants2. Observing 35 populations of the silverweed cinquefoil, Argentina anserine, across a range of latitudes in both hemispheres they saw a clear trend towards greater dark pigmentation in populations from lower latitudes. This pattern is not visible to the casual observer, being due to pigments that observe ultraviolet light.  Gloger’s Rule has had a venerable history, rife with conjectures as to its cause. One explanation is that it arises as an adaptation against feather degradation by bacteria in moister climates3. The pigment responsible for much of the variation in darkness, eumelanin, improves feathers’ resistance to both physical and chemical damage. Other zoologists have noted that various mammal groups also adhere to Gloger’s Rule, at least using latitude as a proxy for climate4,5, but have tended to favour different explanations.   The direct overhead solar illumination of the tropics also produces more intense dorso-ventral shadowing. This is thought to favour stronger countershading (darker back, lighter belly) to counteract the self-shadowing and aid camouflage, as supported by data from a comparative study of ungulates6. Conversely, the favoured explanation for the variation in skin colour in humans is a trade-off between the benefits of protection from UV damage and need for UV for vitamin D3 synthesis7,8. In the tropics the balance is in favour of UV protection and dark skin, at higher latitudes the weaker sun favours reduced pigmentation to allow vitamin D3 synthesis9.  Since Koski and Ashman observed variation in UV pigmentation they could directly test the UV protection hypothesis as it applies to flowers2.  A “bullseye” pattern is common in many flowers, often with the petal bases absorbing UV and the petal tips strongly reflective (see figure). Although attracting and/or guiding pollinating insects is a likely function, a role has been suggested in the protection of pollen from UV light reflected on to the anthers by the disk of petals. Koski and Ashman measured the size of the UV bullseye in their populations of A. anserine. Across four latitudinal transects, bullseye size 2  increased towards the equator. Crucially for the proposed function, the level of UV-B irradiance at each location was the best predictor of bullseye size, followed by temperature but not rainfall.   But does a larger bullseye really protect the flower from UV? Kloski and Ashman took A. anserine plants into the lab and exposed half the flowers of each plant to ecologically realistic levels of UV-B irradiation, with the other half unexposed. In the absence of UV, pollen germination was actually higher in flowers with smaller bullseyes, but in the presence of UV-B the relationship changed, with higher pollen viability from flowers in which they were larger, but not too large. In a second lab experiment, with artificial flowers surrounding the anthers from real plants, flowers with large bullseyes had pollen germination levels similar to that in the absence of UV, while that from flowers with small bullseyes had 28% lower germination rates. These two lab experiments demonstrate that UV-absorbing petal tissue does enhance pollen viability, consistent with the latitudinal variation being the result of selection for UV protection.   This an important conclusion about the causes of floral colour variation, although it does not rule out other factors from being as (or more) significant, including the effects of UV on other plant functions. Nevertheless it is somewhat ironic that, after 180 years of research on Gloger’s rule by zoologists, some of the strongest evidence for the driver of that latitudinal pattern comes from research on plants. It is of course possible that Gloger’s rule has no single explanation and that different groups are responding to different selective agents, all correlated with latitude. After all, Gloger’s original observation was of a relationship between pigmentation and “warmth” as much as latitude.  Also, although for both A. anserine and humans UV-B irradiance is a stronger correlate of pigmentation than humidity or latitude per se, in humans it may be UV-B-induced folate photolysis that is the major selective agent8. What is clear is that, nearly 200 years on, the observations of Constantin Lambert Gloger are still providing inspiration for innovative research.   Innes C. Cuthill is at the School of Biological Sciences, Life Sciences Building, University of Bristol, Bristol BS8 1TQ, UK I.Cuthill@bristol.ac.uk   References  1.  Gloger,	C.	W.	L.	Das	Abändern	der	Vögel	durch	Einfluss	des	Klima's	[The	Evolution	of	Birds	Through	the	Impact	of	Climate]	(in	German)	Accessed	online	http://archive.org/stream/Gloger1833nh20H	-	page/n3/mode/2up.		(August	Schultz	und	Comp.,	1833). 2	 Koski,	M.	H.	&	Ashman,	T.-L.	An	animal	rule	for	flowers.	Nature	Plants	xx,	xx-xx	(2014). 3	 Burtt,	E.	H.	J.	&	Ichida,	J.	M.	Gloger's	Rule,	feather-degrading	bacteria,	and	color	variation	among	Song	Sparrows.	The	Condor	106,	681–686	(2004). 4	 Kamiliar,	J.	M.	&	Bradley,	B.	J.	Interspecific	variation	in	primate	coat	colour	supports	Gloger’s	rule.	Journal	of	Biogeography	38,	2270–2277	(2011). 5	 Stoner,	C.	J.,	Caro,	T.	M.	&	Graham,	C.	M.	Ecological	and	behavioral	correlates	of	coloration	in	artiodactyls:	systematic	analyses	of	conventional	hypotheses.	Behav.	Ecol.	14,	823-840	(2003). 6	 Allen,	W.	L.,	Baddeley,	R.,	Cuthill,	I.	C.	&	Scott-Samuel,	N.	E.	A	quantitative	test	of	the	3  predicted	relationship	between	countershading	and	lighting	environment.	Am.	Nat.	180,	762-776,	doi:10.1086/668011	(2012). 7	 Roberts,	D.	F.	&	Kahlon,	D.	P.	S.	Environmental	correlations	of	skin	colour.	Annals	of	Human	Biology	3,	11–22	(1976). 8	 Chaplin,	G.	Geographic	distribution	of	environmental	factors	influencing	human	skin	coloration.	American	Journal	of	Physical	Anthropology	125,	292–302	(2004). 9	 Jablonski,	N.	G.	&	Chaplin,	G.	Human	skin	pigmentation	as	an	adaptation	to	UV	radiation.	PNAS	107(Suppl	2),	8962–8968	(2010).   Figure 1.  A. anserine flowers showing enlarged UV bullseyes at lower latitudes. Although similar to the naked eye (left) the upper bloom shows a larger area of dark pigmentation under UV light (right). The flowers come from the extreme north (upper) and south (lower) of New Zealand. Image by Matthew Koski.   

Flower colour:Gloger's rule isn't just for the birds

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Flower colour:Gloger's rule isn't just for the birds

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