One of the most important concepts in animal signalling theory, proposed by Amotz Zahavi in a seminal 1975 paper and in later works (Zahavi 1977; Zahavi & Zahavi 1997), is the handicap principle. A general definition is that females have evolved mating preferences for males who display exaggerated ornaments or behaviours that are costly to maintain and develop, and that this cost ensures an ‘honest’ signal of male genetic quality.
As a student I found it quite difficult to identify a working definition for this important type of signal mainly due to the apparent ‘coining fest’ that has taken place over the years since Zahavi outlined his original idea in 1975. For this reason, I have decided to provide a brief outline of the terminological and conceptual differences that exist in relation to the handicap principle in an attempt to help anyone who might be struggling to navigate the literature.
As Zahavi did not define the handicap principle mathematically, a number of interpretations can be found in the key literature due to scholars disagreeing as to the true nature of his original idea. Until John Maynard Smith and Harper simplified and clarified things wonderfully in their 2003 publication Animal Signals, to my knowledge at least four different interpretations of the handicap were being used and explored empirically and through mathematical modelling, each with distinct differences that aren’t all that obvious to grasp without delving into the maths.
Before I describe my understanding of these, it is important to note that each of these handicaps can be classified as good genes handicaps. The good genes model states that sexual traits serve as reliable indicators of a male’s genetic quality rather than a male’s condition as determined by environmental factors. Thus, when I refer to ‘male quality’ I am referring to a scale that concerns differences in genetic quality.
‘Good Genes’ Handicaps
1) Zahavi’s Handicap
Zahavi’s handicap is coined as such because of a general consensus or assumption that this interpretation was the closest to that which Zahavi originally intended. According to Zahavi’s handicap, all males express the handicap despite their level of quality. However, high quality males pay a lesser cost in order to do this than low quality males. The key thing here is that a higher fraction of high quality males survive despite the handicap than low quality males. Thus, high quality males survive longest and mate with more females, increasing the spread of their genes.
2) The Condition-dependent Handicap
As the name suggests, the expression of the condition-dependent handicap is dependent on the genetic condition of the male. In other words, level of display or advertisement of a trait or behaviour is proportional to male quality. For example, a low quality male will express the handicap to a lesser extent than a high quality male. This is because the high quality male is more able to invest the costly energy required in order to express the trait maximally or to a larger extent than the low quality male without adverse effects to fitness.
Unlike Zahavi’s handicap which proposes a ‘fixed’ trait for low and high quality males, the condition-dependent handicap acknowledges that males can express a trait or behaviour to varying degrees and that females discriminate between them on this basis.
3) The Revealing Handicap... or Index
In the case of a revealing handicap as identified and coined by Maynard Smith (1985), honesty is maintained not by cost, but by an inescapable correlation between the nature of the signal and the signaller’s quality making it is impossible to fake. In a way that is similar to the condition-dependent handicap, indices are displayed to varying degrees by males of all viability levels– the intensity of the signal varies on a scale in accordance with level of male quality.
Plumage brightness in Passerine birds as discussed by Hamilton and Zuk in their 1982 paper has often been cited as a classic demonstration of the revealing handicap. It does not cost a male anything to display a bright plumage. This is because the brightness of his plumage is directly affected by parasite load rather than imposing a negative effect on his survival in some way or demanding a large amount of energy from him in order to maintain it. By extension, plumage brightness is still an honest indicator of male quality despite the lack of obvious cost (with regards to his level of genetically determined parasite resistance) as a male cannot fake his parasite load.
Due to the lack of cost as a necessity to make the revealing handicap work, Maynard-Smith and Harper (1995; 2003) later pointed out that it shouldn’t really be considered a handicap at all, as cost is an essential component of the handicap principle. To emphasise this distinction and to eliminate the inevitable confusion that would have followed by sticking to its former name, they re-christened the revealing handicap as an index, a wider term borrowed from the semiotician Charles S. Pierce to describe a signal that is ‘physically connected with its object’.
4) Grafen’s Strategic Choice Handicap
The term ‘strategic choice handicap’ was coined by the biologist Alan Grafen. In 1990 he presented two landmark papers (Grafen 1990b; 1990b) which confirmed the plausibility of the handicap principle mathematically.
The essence of the strategic handicap is that all males have the ‘option’ (an unconscious process) to display a large handicap despite their level of quality. In this sense it is closer to ‘Zahavi’s’ handicap than the condition dependent handicap. However, males must make a ‘choice’ as to how to much they display based on the ‘knowledge’ they have of their own level of quality. The signal remains honest despite this additional element of ‘choice’ because low quality males will never signal at a level that is higher than would be advantageous for them to do so because of the increased cost of display for low relative to high quality males. In this sense, the strategic choice handicap is closer to the condition-dependent handicap in that males of different qualities advertise at different levels.
The Good Parent Handicap
To top it all, there is a fourth type of handicap - the good parent handicap. This works in exactly the same way as Zahavi’s, condition-dependent and strategic choice handicaps with regards to cost being necessary to ensure signal honesty. It exists because several scholars (e.g. Heywood 1989; Hoelzer 1989; Iwasa & Pomiankowski 1999) have argued that exaggerated ornaments and behaviours in fact serve as honest signals of differences in male quality as affected by environmental factors rather than genetic ones.
In this case, the female gains a direct survival benefit by choosing to mate with a male who is in good condition and who can provide her with material benefits such as parental care (hence the name of this type of handicap), absence of parasitism and other resources. A male’s handicap level and ability to do this is determined by his quality which is in turn affected by environmental factors (i.e. availability of resources, parasite prevalence).
The next post on this topic will be a short discussion of how the general terms ‘handicap’ and ‘index’ have been applied to examples in nature. I will also highlight some ambiguous and problematic cases where it has proven difficult to classify traits in this manner.
Grafen, A. (1990a) Biological Signals as Handicaps. Journal of Theoretical Biology 144, 517-546.
Grafen, A. (1990b) Sexual Selection Unhandicapped by the Fisher Process. Journal of Theoretical Biology 144, 437-516.
Hamilton, W.D. and M. Zuk. 1982. Heritable true fitness and bright birds: a role for parasites? Science 218: 384-387.
Heywood, J. S. (1989) Sexual selection by the handicap mechanism. Evolution 43: 1387-1397.
Hoelzer, G. A. (1989) The good parent process of sexual selection. Animal Behaviour. 38, 1067-1078.
Iwasa, Y. and Pomiankowski, A. (1999) Good Parent and Good Genes Models of Handicap Evolution. Journal of Theoretical Biology 200, 97-109.
Maynard Smith, J. (1985) Sexual selection, handicaps and true fitness. Journal of Theoretical Biology 115, 1-8.
Maynard Smith, J. and Harper, D. G. C. (1995) Animal Signals: Models and Terminology. Journal of Theoretical Biology 177, 305-311.
Maynard Smith, J. and Harper, D. G. C. (2003) Animal Signals. Oxford: Oxford University Press.
Zahavi, A. (1975) Mate selection – A selection for a handicap. Journal of Theoretical Biology 53, 205-214.
Zahavi, A. (1977) The cost of honesty (Further remarks on the handicap principle). Journal of Theoretical Biology 67, 603-605
Zahavi, A and Zahavi, A. (1997) The Handicap Principle: A Missing Piece of Darwin’s Puzzle. New York: Oxford University Press.
ZAHAVI, A. (1975). Mate selection?A selection for a handicap Journal of Theoretical Biology, 53 (1), 205-214 DOI: 10.1016/0022-5193(75)90111-3