- Email: [email protected]
Evolutionary Ecology: Knowing How to Hide Your Eggs
Current Biology Vol 23 No 3 R106
production, might be considered. For instance, this balance can be tipped towards Rac effects by statin drugs [12] acting through their somewhat more selective inhibition of Rho activation. If so, perhaps statins could decrease the sensitization phase in the murine hypersensitivity model employed here, and perhaps even in some circumstances in human asthma. While therapeutics for allergic asthma, particularly inhaled corticosteroids, are largely effective in treating established disease, none currently targets the initial sensitization steps. Thus, enhancing airway epithelial Rac may be a novel target in early intervention, or even prevention, of this disease.
3.
4.
5.
6.
7.
References 1. Lettre, G., and Hengartner, M.O. (2006). Developmental apoptosis in C. elegans: a complex CEDnario. Nat. Rev. Mol. Cell Biol. 7, 97–108. 2. Scott, R.S., McMahon, E.J., Pop, S.M., Reap, E.A., Caricchio, R., Cohen, P.L.,
8.
Earp, H.S., and Matsushima, G.K. (2001). Phagocytosis and clearance of apoptotic cells is mediated by MER. Nature 411, 207–211. Fadok, V.A., Voelker, D.R., Campbell, P.A., Cohen, J.J., Bratton, D.L., and Henson, P.M. (1992). Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 148, 2207–2216. Gardai, S.J., Bratton, D.L., Ogden, C.A., and Henson, P.M. (2006). Recognition ligands on apoptotic cells: a perspective. J. Leukoc. Biol. 79, 896–903. Monks, J., Smith-Steinhart, C., Kruk, E.R., Fadok, V.A., and Henson, P.M. (2008). Epithelial cells remove apoptotic epithelial cells during post-lactation involution of the mouse mammary gland. Biol. Reprod. 78, 586–594. Fadok, V.A., Bratton, D.L., Konowal, A., Freed, P.W., Westcott, J.Y., and Henson, P.M. (1998). Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/ paracrine mechanisms involving TGF-beta, PGE2, and PAF. J. Clin. Invest. 101, 890–898. Juncadella, I.J., Kadl, A., Sharma, A.K., Shim, Y.M., Hochreiter-Hufford, A., Borish, L., and Ravichandran, K.S. (2012). Apoptotic cell clearance by bronchial epithelial cells critically influences airway inflammation. Nature http://dx.doi.org/10.1038/nature11714. Sexton, D.W., Al-Rabia, M., Blaylock, M.G., and Walsh, G.M. (2004). Phagocytosis of apoptotic eosinophils but not neutrophils by bronchial epithelial cells. Clin. Exp. Allergy 34, 1514–1524.
Evolutionary Ecology: Knowing How to Hide Your Eggs A new study of camouflage in quail shows that individual birds know the appearance of their own eggs and select backgrounds that maximise concealment. Martin Stevens The study of camouflage has been a central feature of evolutionary theory since Darwin and Wallace [1,2], exemplified by the classic textbook example of evolution: the peppered moth [3,4]. As a phenomenon, camouflage seems intuitively simple — one only needs to find a hidden stick insect or cuttlefish to appreciate its function. Only in the last decade, however, have scientists really got to grips with the different forms of camouflage that exist, tested the survival value that they confer, and how they work in terms of visual processing. In this time, the first experimental support has been found for almost all types of camouflage [5–7], despite most theories existing for more than 100 years [8]. The emphasis in most research has been on the optimization
and tuning of camouflage coloration over successive generations, yet it is well known that individuals of various species, for example many moths, show species-level behavioural preferences for particular backgrounds to rest on [9,10]. But little work has tested whether individuals within a species actively chose backgrounds or microhabitats that best confer camouflage with regards to their own specific appearance. In this issue of Current Biology, Lovell et al. [11] report that individual Japanese quail (Coturnix japonica), when given a choice of substrates of different colours, select the background to lay their eggs on that confers the best camouflage. Lovell et al.’s [11] experiment showed that the individual quail choices were dependent on the appearance of their own eggs, specifically how maculated (patterned)
9. Vandivier, R.W., Richens, T.R., Horstmann, S.A., deCathelineau, A.M., Ghosh, M., Reynolds, S.D., Xiao, Y.Q., Riches, D.W., Plumb, J., Vachon, E., et al. (2009). Dysfunctional cystic fibrosis transmembrane conductance regulator inhibits phagocytosis of apoptotic cells with proinflammatory consequences. Am. J. Physiol. Lung Cell Mol. Physiol 297, L677–L686. 10. Sander, E.E., ten Klooster, J.P., van Delft, S., van der Kammen, R.A., and Collard, J.G. (1999). Rac downregulates Rho activity: reciprocal balance between both GTPases determines cellular morphology and migratory behavior. J. Cell Biol. 147, 1009–1022. 11. Ridley, A.J. (2001). Rho family proteins: coordinating cell responses. Trends Cell Biol. 11, 471–477. 12. Morimoto, K., Janssen, W.J., Fessler, M.B., McPhillips, K.A., Borges, V.M., Bowler, R.P., Xiao, Y.Q., Kench, J.A., Henson, P.M., and Vandivier, R.W. (2006). Lovastatin enhances clearance of apoptotic cells (efferocytosis) with implications for chronic obstructive pulmonary disease. J. Immunol. 176, 7657–7665.
Program in Cell Biology, Department of Pediatrics, National Jewish Health, 1400 Jackson St, Denver, CO 80206 USA. E-mail: [email protected], Brattond@ njhealth.org http://dx.doi.org/10.1016/j.cub.2012.12.008
they are. Individuals with eggs having lots of dark maculation (up to around 50% of the egg surface) selected backgrounds that were dark, and this provided improved concealment through disruptive coloration (breaking up the appearance of body outlines [1,12]) as the dark markings blended into the backgroundand broke up the egg shape. Conversely, individuals with few markings and generally light coloured eggs chose light coloured backgrounds that provided camouflage by background matching (simply matching the colour and pattern of the substrate). This new study has a number of important implications. First, effective camouflage can be a product not just of tuning of appearance over multiple generations, but also the behavioural choices of individual animals. A study of camouflage that simply compares all individuals to randomly chosen background samples could be inappropriate if different individuals show preferences for specific microhabitats that optimize their own concealment. This could be especially important in highly mobile species. A next step in this area of work is to test what specific cues individuals
Dispatch R107
might use to select particular background types. Second, the majority of research testing camouflage types has been undertaken in artificial systems or with modelling. Lovell et al.’s [11] study provides evidence for the use of disruptive coloration in real species, something that has rarely been demonstrated or tested outside of artificial paradigms [12]. Work now needs to test these findings in more natural systems with real backgrounds and free-living species. Also, this study based the analysis of egg coloration on human vision metrics, even though the real predators of quail are likely to have quite different visual systems. The results are unlikely to be greatly changed, but we need to test effects of background selection on predator detection (both behaviourally, and by modelling predator vision). This is something that applies broadly — determining the value of camouflage in real species in reducing detection from real predators (and knowing what those predators actually are) in natural systems remains a major challenge. Furthermore, for field studies, being sure of where most individuals rest can be difficult. By definition, camouflaged species are hard to find (!) and so obtaining sufficient sample sizes is tough. It is difficult to know whether the individuals that we find are just anomalies that happen to have rested in inappropriate places or are truly representative of the species. Using ground nesting birds avoids this problem because their nesting sites are relatively easy to find and are well documented (Figure 1). One of the more far-reaching implications of Lovell et al.’s [11] study is that individual quail ‘know’ the appearance of their own eggs, and this has important parallels with other systems. For example, many hosts of avian brood parasites seem to have an internal ‘template’ of their own egg appearance. Instead of simply rejecting the odd egg out in a clutch, which is likely to be the parasite’s, hosts often reject foreign eggs that deviate sufficiently from their template [13]. A major gap in our understanding, however, is the exact form of these templates and whether they are ‘innate’ (inherited) or if individuals learn the appearance of their eggs in their initial breeding attempts. If egg appearance is learnt, determining which aspects of
egg appearance is memorized and for how long will be valuable [14]. Because of the complex nature of most brood parasitic systems, experiments distinguishing between such ideas are highly challenging because they involve wild birds in the field, where the age and level of experience of the breeders is rarely known and other factors are hard to control. Egg camouflage and background selection in birds like quail that are easier to keep in captivity could be a tractable alternative because individuals can be raised in the lab, with the egg coloration and background selection of their mothers tested, along with the choices of naı¨ve first time breeders. Other recent lab work with Japanese quail, which may suffer both from intraspecific brood parasitism and a need to camouflage their eggs from predators, shows that females can be taught to recognize egg appearance and use specific features of this to discriminate between unfamiliar eggs [15]. But the task in this study was not particularly closely related to natural problems quail face (for example, rejection behaviour). Lovell et al.’s [11] study and subsequent work can also tell us much about how different camouflage and associated behavioural strategies evolve, and even have implications for larger scale evolutionary changes. Variation in potential resting backgrounds within a habitat could lead to several potential outcomes in camouflage strategy in a species. First, all individuals could specialize on one background type alone (for example the most common type or where predation risk is greatest) but have poor camouflage on other backgrounds. Second, all individuals could adopt an appearance that resembles features of each background type but that matches none closely (‘compromise camouflage’ [16]). Third, polymorphism could arise, whereby different morphs specialise on and closely resemble particular substrates or microhabitats. This latter possibility occurs in some insects [17,18], although may sometimes arise from phenotypic plasticity. Little work has investigated how individuals select appropriate backgrounds or how differences between individuals first arise. Furthermore, whether individual selection of background types exists in species with more continuous variation
Figure 1. Camouflage in bird eggs. Ground nesting birds such as the bronzewing courser (Rhinoptilus chalcopterus; top) and Mozambique nightjar (Caprimulgus fossii; bottom) make excellent systems to study camouflage and substrate selection because the resting background is often well known and the eggs need to be camouflaged directly against the substrate that has been chosen.
among individuals is poorly known. In birds, if behavioural choice and egg coloration are heritable and linked (in most avian species, egg appearance at least is strongly heritable), then distinct lines of individuals could arise that specialize on different microhabitats. Again, this has clear parallels with many brood parasites, where individual females (‘host races’ or gentes) within a species specialize on parasitizing the eggs of different host species, allowing refined mimicry of host eggs to evolve [19]. This can lead to intraspecific polymorphism in egg coloration. Background specialization and polymorphism in camouflaged species could, therefore, sometimes parallel host races in brood parasites. Tantalisingly, there is evidence from some camouflaged species, where individuals live on different substrate
Current Biology Vol 23 No 3 R108
types, that disruptive selection can lead to divergence and even speciation because intermediate forms match neither substrate effectively and are selected against [17]. Interestingly, parasitic cuckoos show higher rates of speciation than non-parasitic species [20], and this may occur if different host races no longer interbreed if this breaks up sophisticated egg mimicry and other host species-specific specializations. Such processes could start to arise in ground nesting birds too if individuals start to specialize on particular distinct microhabitats. Clearly, camouflage is much more than simply a wonderful example of evolution; it can tell us a great deal about the optimization of phenotype and behaviour, macro- and micro-evolutionary processes, and mechanisms such as molecular biology and visual perception.
10.
References
11.
1. Stevens, M., and Merilaita, S. (2009). Introduction. Animal camouflage: current issues and new perspectives. Phil. Trans. R. Soc. B. 364, 423–427. 2. Wallace, A.R. (1889). Darwinism. An Exposition of the Theory of Natural Selection
3.
4.
5.
6.
7.
8.
9.
12.
With Some of its Applications (London: Macmillan & Co). Cook, L.M., Grant, B.S., Saccheri, I.J., and Mallet, J. (2012). Selective bird predation on the peppered moth: the last experiment of Michael Majerus. Biol. Lett. 8, 609–612. Kettlewell, H.B.D. (1955). Selection experiments on industrial melanism in the Lepidoptera. Heredity 9, 323–342. Cuthill, I.C., Stevens, M., Sheppard, J., Maddocks, T., Pa´rraga, C.A., and Troscianko, T.S. (2005). Disruptive coloration and background pattern matching. Nature 434, 72–74. Rowland, H.M., Speed, M.P., Ruxton, G.D., Edmunds, M., Stevens, M., and Harvey, I.F. (2007). Countershading enhances cryptic protection: an experiment with wild birds and artificial prey. Anim. Behav. 74, 1249–1258. Skelhorn, J., Rowland, H.M., Speed, M.P., and Ruxton, G.D. (2010). Masquerade: Camouflage without crypsis. Science 327, 51. Thayer, G.H. (1909). Concealing-Coloration in the Animal Kingdom: An Exposition of the Laws of Disguise Through Color and Pattern: Being a Summary of Abbott H. Thayer’s Discoveries (New York: Macmillan). Kang, C.-K., Moon, J.-Y., Lee, S.-I., and Jablonski, P.G. (2012). Camouflage through an active choice of a resting spot and body orientation in moths. J. Evol. Biol. 25, 1695–1702. Sargent, T.D. (1966). Background selections of geometrid and noctuid moths. Science 154, 1674–1675. Lovell, P.G., Ruxton, G.D., Langridge, K.V., and Spencer, K.A. (2013). Egg-laying substrate selection for optimal camouflage by quail. Curr. Biol. 23, 260–264. Stevens, M., and Merilaita, S. (2009). Defining disruptive coloration and distinguishing its functions. Phil. Trans. R. Soc. B. 364, 481–488.
Microbiology: EHEC Downregulates Virulence in Response to Intestinal Fucose Recent work has revealed that enterohaemorrhagic Escherichia coli encodes a two-component system, termed FusKR, which responds to fucose and represses expression of virulence genes. Furthermore, a representative member of the microbiota appears to cleave fucose from host glycans, indicating that the microbiota and EHEC may act in concert to suppress virulence gene expression. Kristie M. Keeney and B. Brett Finlay The environmental signals that trigger enterohaemorrhagic Escherichia coli (EHEC) to begin its virulent life cycle within the large intestine of its human host are beginning to be explored, yielding a better understanding of the early stages of this pathogen’s strategy to colonize its host. Expression of the type III secretion system (T3SS) by EHEC is essential for virulence, enabling it to attach to the host by forming attaching and effacing lesions [1]. Attaching and effacing lesions are
characterized by effacement (loss) of the intestinal microvilli and intimate attachment of the pathogen to the epithelial cell with pedestal-like structures underlying the bacterium [1]. The genes encoding the T3SS are located within a genetic island termed the locus of enterocyte effacement (LEE), which is under the control of a master regulator, Ler [1]. Following on from their earlier studies, the Sperandio group [2] now present a model for initial EHEC intestinal colonization, whereby fucose freed from the mucus layer by a member of the microbiota,
13. Rothstein, S.I. (1975). Mechanisms of avian egg-recognition: do birds know their own eggs. Anim. Behav. 23, 268–278. 14. Petrie, M., Pinxten, R., and Eens, M. (2009). Moorhens have an internal representation of their own eggs. Naturwissenschaften 96, 405–407. 15. Pike, T.W. (2011). Egg recognition in quail. Avian Biol. Res. 4, 231–236. 16. Merilaita, S., Tuomi, J., and Jormalainen, V. (1999). Optimization of cryptic coloration in heterogeneous habitats. Biol. J. Linn. Soc. 67, 151–161. 17. Nosil, P., and Crespi, B.J. (2006). Experimental evidence that predation promotes divergence in adaptive radiation. Proc. Natl. Acad. Sci. USA 103, 9090–9095. 18. Pellissier, L., Wassef, J., Bilat, J., Brazzola, G., Buri, P., Colliard, C., Fournier, B., Hausser, J., Yannic, G., and Perrin, N. (2011). Adaptive colour polymorphism of Acrida ungarica H. (Orthoptera: Acrididae) in a spatially heterogeneous environment. Acta Oecol. 37, 93–98. 19. Stoddard, M.C., and Stevens, M. (2011). Avian vision and the evolution of egg color mimicry in the common cuckoo. Evolution 65, 2004–2013. 20. Kru¨ger, O., Sorenson, M.D., and Davies, N.B. (2009). Does coevolution promote species richness in parasitic cuckoos? Proc. R. Soc. Lond. B. 276, 3871–3879.
Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UK. E-mail: [email protected] http://dx.doi.org/10.1016/j.cub.2012.12.009
Bacteroidetes thetaiotamicron, inhibits LEE expression, relieving the pathogen from the metabolic burden of expressing the T3SS and giving it a competitive growth advantage in the lumen of the gut. Once EHEC approaches the mucosal surface, adrenergic metabolites de-repress the LEE, initiating its adherence mechanisms (Figure 1). Prior work from this group showed that, upon exposure to external host adrenergic signals and the microbiota-generated autoinducer signal AI-3, two histidine sensor kinases undergo autophosphorylation and relay their phosphate to response regulators that enhance EHEC virulence [3,4]. In addition to what was already known about the promotion of virulence phenotypes by AI-3 and adrenergic signals, the new study reports that two of these response regulators also repress expression of the FusKR two-component system, where FusK is the histidine sensor kinase and FusR the response regulator. This repression promotes virulence, since the presence of both
production, might be considered. For instance, this balance can be tipped towards Rac effects by statin drugs [12] acting through their somewhat more selective inhibition of Rho activation. If so, perhaps statins could decrease the sensitization phase in the murine hypersensitivity model employed here, and perhaps even in some circumstances in human asthma. While therapeutics for allergic asthma, particularly inhaled corticosteroids, are largely effective in treating established disease, none currently targets the initial sensitization steps. Thus, enhancing airway epithelial Rac may be a novel target in early intervention, or even prevention, of this disease.
3.
4.
5.
6.
7.
References 1. Lettre, G., and Hengartner, M.O. (2006). Developmental apoptosis in C. elegans: a complex CEDnario. Nat. Rev. Mol. Cell Biol. 7, 97–108. 2. Scott, R.S., McMahon, E.J., Pop, S.M., Reap, E.A., Caricchio, R., Cohen, P.L.,
8.
Earp, H.S., and Matsushima, G.K. (2001). Phagocytosis and clearance of apoptotic cells is mediated by MER. Nature 411, 207–211. Fadok, V.A., Voelker, D.R., Campbell, P.A., Cohen, J.J., Bratton, D.L., and Henson, P.M. (1992). Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 148, 2207–2216. Gardai, S.J., Bratton, D.L., Ogden, C.A., and Henson, P.M. (2006). Recognition ligands on apoptotic cells: a perspective. J. Leukoc. Biol. 79, 896–903. Monks, J., Smith-Steinhart, C., Kruk, E.R., Fadok, V.A., and Henson, P.M. (2008). Epithelial cells remove apoptotic epithelial cells during post-lactation involution of the mouse mammary gland. Biol. Reprod. 78, 586–594. Fadok, V.A., Bratton, D.L., Konowal, A., Freed, P.W., Westcott, J.Y., and Henson, P.M. (1998). Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/ paracrine mechanisms involving TGF-beta, PGE2, and PAF. J. Clin. Invest. 101, 890–898. Juncadella, I.J., Kadl, A., Sharma, A.K., Shim, Y.M., Hochreiter-Hufford, A., Borish, L., and Ravichandran, K.S. (2012). Apoptotic cell clearance by bronchial epithelial cells critically influences airway inflammation. Nature http://dx.doi.org/10.1038/nature11714. Sexton, D.W., Al-Rabia, M., Blaylock, M.G., and Walsh, G.M. (2004). Phagocytosis of apoptotic eosinophils but not neutrophils by bronchial epithelial cells. Clin. Exp. Allergy 34, 1514–1524.
Evolutionary Ecology: Knowing How to Hide Your Eggs A new study of camouflage in quail shows that individual birds know the appearance of their own eggs and select backgrounds that maximise concealment. Martin Stevens The study of camouflage has been a central feature of evolutionary theory since Darwin and Wallace [1,2], exemplified by the classic textbook example of evolution: the peppered moth [3,4]. As a phenomenon, camouflage seems intuitively simple — one only needs to find a hidden stick insect or cuttlefish to appreciate its function. Only in the last decade, however, have scientists really got to grips with the different forms of camouflage that exist, tested the survival value that they confer, and how they work in terms of visual processing. In this time, the first experimental support has been found for almost all types of camouflage [5–7], despite most theories existing for more than 100 years [8]. The emphasis in most research has been on the optimization
and tuning of camouflage coloration over successive generations, yet it is well known that individuals of various species, for example many moths, show species-level behavioural preferences for particular backgrounds to rest on [9,10]. But little work has tested whether individuals within a species actively chose backgrounds or microhabitats that best confer camouflage with regards to their own specific appearance. In this issue of Current Biology, Lovell et al. [11] report that individual Japanese quail (Coturnix japonica), when given a choice of substrates of different colours, select the background to lay their eggs on that confers the best camouflage. Lovell et al.’s [11] experiment showed that the individual quail choices were dependent on the appearance of their own eggs, specifically how maculated (patterned)
9. Vandivier, R.W., Richens, T.R., Horstmann, S.A., deCathelineau, A.M., Ghosh, M., Reynolds, S.D., Xiao, Y.Q., Riches, D.W., Plumb, J., Vachon, E., et al. (2009). Dysfunctional cystic fibrosis transmembrane conductance regulator inhibits phagocytosis of apoptotic cells with proinflammatory consequences. Am. J. Physiol. Lung Cell Mol. Physiol 297, L677–L686. 10. Sander, E.E., ten Klooster, J.P., van Delft, S., van der Kammen, R.A., and Collard, J.G. (1999). Rac downregulates Rho activity: reciprocal balance between both GTPases determines cellular morphology and migratory behavior. J. Cell Biol. 147, 1009–1022. 11. Ridley, A.J. (2001). Rho family proteins: coordinating cell responses. Trends Cell Biol. 11, 471–477. 12. Morimoto, K., Janssen, W.J., Fessler, M.B., McPhillips, K.A., Borges, V.M., Bowler, R.P., Xiao, Y.Q., Kench, J.A., Henson, P.M., and Vandivier, R.W. (2006). Lovastatin enhances clearance of apoptotic cells (efferocytosis) with implications for chronic obstructive pulmonary disease. J. Immunol. 176, 7657–7665.
Program in Cell Biology, Department of Pediatrics, National Jewish Health, 1400 Jackson St, Denver, CO 80206 USA. E-mail: [email protected], Brattond@ njhealth.org http://dx.doi.org/10.1016/j.cub.2012.12.008
they are. Individuals with eggs having lots of dark maculation (up to around 50% of the egg surface) selected backgrounds that were dark, and this provided improved concealment through disruptive coloration (breaking up the appearance of body outlines [1,12]) as the dark markings blended into the backgroundand broke up the egg shape. Conversely, individuals with few markings and generally light coloured eggs chose light coloured backgrounds that provided camouflage by background matching (simply matching the colour and pattern of the substrate). This new study has a number of important implications. First, effective camouflage can be a product not just of tuning of appearance over multiple generations, but also the behavioural choices of individual animals. A study of camouflage that simply compares all individuals to randomly chosen background samples could be inappropriate if different individuals show preferences for specific microhabitats that optimize their own concealment. This could be especially important in highly mobile species. A next step in this area of work is to test what specific cues individuals
Dispatch R107
might use to select particular background types. Second, the majority of research testing camouflage types has been undertaken in artificial systems or with modelling. Lovell et al.’s [11] study provides evidence for the use of disruptive coloration in real species, something that has rarely been demonstrated or tested outside of artificial paradigms [12]. Work now needs to test these findings in more natural systems with real backgrounds and free-living species. Also, this study based the analysis of egg coloration on human vision metrics, even though the real predators of quail are likely to have quite different visual systems. The results are unlikely to be greatly changed, but we need to test effects of background selection on predator detection (both behaviourally, and by modelling predator vision). This is something that applies broadly — determining the value of camouflage in real species in reducing detection from real predators (and knowing what those predators actually are) in natural systems remains a major challenge. Furthermore, for field studies, being sure of where most individuals rest can be difficult. By definition, camouflaged species are hard to find (!) and so obtaining sufficient sample sizes is tough. It is difficult to know whether the individuals that we find are just anomalies that happen to have rested in inappropriate places or are truly representative of the species. Using ground nesting birds avoids this problem because their nesting sites are relatively easy to find and are well documented (Figure 1). One of the more far-reaching implications of Lovell et al.’s [11] study is that individual quail ‘know’ the appearance of their own eggs, and this has important parallels with other systems. For example, many hosts of avian brood parasites seem to have an internal ‘template’ of their own egg appearance. Instead of simply rejecting the odd egg out in a clutch, which is likely to be the parasite’s, hosts often reject foreign eggs that deviate sufficiently from their template [13]. A major gap in our understanding, however, is the exact form of these templates and whether they are ‘innate’ (inherited) or if individuals learn the appearance of their eggs in their initial breeding attempts. If egg appearance is learnt, determining which aspects of
egg appearance is memorized and for how long will be valuable [14]. Because of the complex nature of most brood parasitic systems, experiments distinguishing between such ideas are highly challenging because they involve wild birds in the field, where the age and level of experience of the breeders is rarely known and other factors are hard to control. Egg camouflage and background selection in birds like quail that are easier to keep in captivity could be a tractable alternative because individuals can be raised in the lab, with the egg coloration and background selection of their mothers tested, along with the choices of naı¨ve first time breeders. Other recent lab work with Japanese quail, which may suffer both from intraspecific brood parasitism and a need to camouflage their eggs from predators, shows that females can be taught to recognize egg appearance and use specific features of this to discriminate between unfamiliar eggs [15]. But the task in this study was not particularly closely related to natural problems quail face (for example, rejection behaviour). Lovell et al.’s [11] study and subsequent work can also tell us much about how different camouflage and associated behavioural strategies evolve, and even have implications for larger scale evolutionary changes. Variation in potential resting backgrounds within a habitat could lead to several potential outcomes in camouflage strategy in a species. First, all individuals could specialize on one background type alone (for example the most common type or where predation risk is greatest) but have poor camouflage on other backgrounds. Second, all individuals could adopt an appearance that resembles features of each background type but that matches none closely (‘compromise camouflage’ [16]). Third, polymorphism could arise, whereby different morphs specialise on and closely resemble particular substrates or microhabitats. This latter possibility occurs in some insects [17,18], although may sometimes arise from phenotypic plasticity. Little work has investigated how individuals select appropriate backgrounds or how differences between individuals first arise. Furthermore, whether individual selection of background types exists in species with more continuous variation
Figure 1. Camouflage in bird eggs. Ground nesting birds such as the bronzewing courser (Rhinoptilus chalcopterus; top) and Mozambique nightjar (Caprimulgus fossii; bottom) make excellent systems to study camouflage and substrate selection because the resting background is often well known and the eggs need to be camouflaged directly against the substrate that has been chosen.
among individuals is poorly known. In birds, if behavioural choice and egg coloration are heritable and linked (in most avian species, egg appearance at least is strongly heritable), then distinct lines of individuals could arise that specialize on different microhabitats. Again, this has clear parallels with many brood parasites, where individual females (‘host races’ or gentes) within a species specialize on parasitizing the eggs of different host species, allowing refined mimicry of host eggs to evolve [19]. This can lead to intraspecific polymorphism in egg coloration. Background specialization and polymorphism in camouflaged species could, therefore, sometimes parallel host races in brood parasites. Tantalisingly, there is evidence from some camouflaged species, where individuals live on different substrate
Current Biology Vol 23 No 3 R108
types, that disruptive selection can lead to divergence and even speciation because intermediate forms match neither substrate effectively and are selected against [17]. Interestingly, parasitic cuckoos show higher rates of speciation than non-parasitic species [20], and this may occur if different host races no longer interbreed if this breaks up sophisticated egg mimicry and other host species-specific specializations. Such processes could start to arise in ground nesting birds too if individuals start to specialize on particular distinct microhabitats. Clearly, camouflage is much more than simply a wonderful example of evolution; it can tell us a great deal about the optimization of phenotype and behaviour, macro- and micro-evolutionary processes, and mechanisms such as molecular biology and visual perception.
10.
References
11.
1. Stevens, M., and Merilaita, S. (2009). Introduction. Animal camouflage: current issues and new perspectives. Phil. Trans. R. Soc. B. 364, 423–427. 2. Wallace, A.R. (1889). Darwinism. An Exposition of the Theory of Natural Selection
3.
4.
5.
6.
7.
8.
9.
12.
With Some of its Applications (London: Macmillan & Co). Cook, L.M., Grant, B.S., Saccheri, I.J., and Mallet, J. (2012). Selective bird predation on the peppered moth: the last experiment of Michael Majerus. Biol. Lett. 8, 609–612. Kettlewell, H.B.D. (1955). Selection experiments on industrial melanism in the Lepidoptera. Heredity 9, 323–342. Cuthill, I.C., Stevens, M., Sheppard, J., Maddocks, T., Pa´rraga, C.A., and Troscianko, T.S. (2005). Disruptive coloration and background pattern matching. Nature 434, 72–74. Rowland, H.M., Speed, M.P., Ruxton, G.D., Edmunds, M., Stevens, M., and Harvey, I.F. (2007). Countershading enhances cryptic protection: an experiment with wild birds and artificial prey. Anim. Behav. 74, 1249–1258. Skelhorn, J., Rowland, H.M., Speed, M.P., and Ruxton, G.D. (2010). Masquerade: Camouflage without crypsis. Science 327, 51. Thayer, G.H. (1909). Concealing-Coloration in the Animal Kingdom: An Exposition of the Laws of Disguise Through Color and Pattern: Being a Summary of Abbott H. Thayer’s Discoveries (New York: Macmillan). Kang, C.-K., Moon, J.-Y., Lee, S.-I., and Jablonski, P.G. (2012). Camouflage through an active choice of a resting spot and body orientation in moths. J. Evol. Biol. 25, 1695–1702. Sargent, T.D. (1966). Background selections of geometrid and noctuid moths. Science 154, 1674–1675. Lovell, P.G., Ruxton, G.D., Langridge, K.V., and Spencer, K.A. (2013). Egg-laying substrate selection for optimal camouflage by quail. Curr. Biol. 23, 260–264. Stevens, M., and Merilaita, S. (2009). Defining disruptive coloration and distinguishing its functions. Phil. Trans. R. Soc. B. 364, 481–488.
Microbiology: EHEC Downregulates Virulence in Response to Intestinal Fucose Recent work has revealed that enterohaemorrhagic Escherichia coli encodes a two-component system, termed FusKR, which responds to fucose and represses expression of virulence genes. Furthermore, a representative member of the microbiota appears to cleave fucose from host glycans, indicating that the microbiota and EHEC may act in concert to suppress virulence gene expression. Kristie M. Keeney and B. Brett Finlay The environmental signals that trigger enterohaemorrhagic Escherichia coli (EHEC) to begin its virulent life cycle within the large intestine of its human host are beginning to be explored, yielding a better understanding of the early stages of this pathogen’s strategy to colonize its host. Expression of the type III secretion system (T3SS) by EHEC is essential for virulence, enabling it to attach to the host by forming attaching and effacing lesions [1]. Attaching and effacing lesions are
characterized by effacement (loss) of the intestinal microvilli and intimate attachment of the pathogen to the epithelial cell with pedestal-like structures underlying the bacterium [1]. The genes encoding the T3SS are located within a genetic island termed the locus of enterocyte effacement (LEE), which is under the control of a master regulator, Ler [1]. Following on from their earlier studies, the Sperandio group [2] now present a model for initial EHEC intestinal colonization, whereby fucose freed from the mucus layer by a member of the microbiota,
13. Rothstein, S.I. (1975). Mechanisms of avian egg-recognition: do birds know their own eggs. Anim. Behav. 23, 268–278. 14. Petrie, M., Pinxten, R., and Eens, M. (2009). Moorhens have an internal representation of their own eggs. Naturwissenschaften 96, 405–407. 15. Pike, T.W. (2011). Egg recognition in quail. Avian Biol. Res. 4, 231–236. 16. Merilaita, S., Tuomi, J., and Jormalainen, V. (1999). Optimization of cryptic coloration in heterogeneous habitats. Biol. J. Linn. Soc. 67, 151–161. 17. Nosil, P., and Crespi, B.J. (2006). Experimental evidence that predation promotes divergence in adaptive radiation. Proc. Natl. Acad. Sci. USA 103, 9090–9095. 18. Pellissier, L., Wassef, J., Bilat, J., Brazzola, G., Buri, P., Colliard, C., Fournier, B., Hausser, J., Yannic, G., and Perrin, N. (2011). Adaptive colour polymorphism of Acrida ungarica H. (Orthoptera: Acrididae) in a spatially heterogeneous environment. Acta Oecol. 37, 93–98. 19. Stoddard, M.C., and Stevens, M. (2011). Avian vision and the evolution of egg color mimicry in the common cuckoo. Evolution 65, 2004–2013. 20. Kru¨ger, O., Sorenson, M.D., and Davies, N.B. (2009). Does coevolution promote species richness in parasitic cuckoos? Proc. R. Soc. Lond. B. 276, 3871–3879.
Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UK. E-mail: [email protected] http://dx.doi.org/10.1016/j.cub.2012.12.009
Bacteroidetes thetaiotamicron, inhibits LEE expression, relieving the pathogen from the metabolic burden of expressing the T3SS and giving it a competitive growth advantage in the lumen of the gut. Once EHEC approaches the mucosal surface, adrenergic metabolites de-repress the LEE, initiating its adherence mechanisms (Figure 1). Prior work from this group showed that, upon exposure to external host adrenergic signals and the microbiota-generated autoinducer signal AI-3, two histidine sensor kinases undergo autophosphorylation and relay their phosphate to response regulators that enhance EHEC virulence [3,4]. In addition to what was already known about the promotion of virulence phenotypes by AI-3 and adrenergic signals, the new study reports that two of these response regulators also repress expression of the FusKR two-component system, where FusK is the histidine sensor kinase and FusR the response regulator. This repression promotes virulence, since the presence of both