Flashy outfits to impress the girls – a means to the end?   Sexual selection and ‘evolutionary suicide’

 

Susan Atkins

Review of: Kokko and Brooks. (2003). Sexy to die for? Sexual selection and the risk of extinction. Ann. Zool. Fennici 40:207-219

 

 

          Kokko and Brooks (2003) sought to examine the link that may exist between sexual selection in a species, and the possible extinction of that species. They adopted a method of presenting their own models and supporting them with previous studies, in conjunction with presenting possible alternative suggestions. They emphasised demography, the analysis of populations and their distribution, in particular.

         While Kokko and Brooks showed how sexual selection could potentially lead a population to extinction, they also showed how it could act in conjunction with natural selection, thus assisting population survival. As a result of myriad studies supporting both sides of any given hypothesis, Kokko and Brooks were led through a knot of opposing logic. Their paper is at once a short review of the subject, a presentation of their own work, but above all it highlights the gaps in current knowledge that need to be filled with empirical work.

        Three possible routes were presented for the development of traits that will have a negative effect on the individual:

a)      competition between males

b)      the overall effect that females have when choosing partners (as opposed to having been chosen or won by males). She may favour male traits that ultimately lower male viability and survival

c)      inter-gender conflict as a result of sexual selection.

The authors focus on sexual selection, so the last two options were discussed in this paper.

 

        If the idea that sexual selection could lead to extinction seems counter-intuitive, it is important to remember that sexual selection is concerned only with reproductive success, while natural selection deals with evolutionary success, the former being “less rigorous” than the latter (Darwin, 1859). As illustration, the authors cited research on dioecious insect-pollinated plants (Vamosi and Otto, 2002). If plenty pollinators are available, there is no pressure on female plants to produce pretty flowers. This leads to a dimorphism, with the male flowers being more attractive than females. In turn, if pollinators become rare, the females receive less insect-attention – and therefore pollen. The ensuing drop in fecundity makes extinction a real threat. The authors asked why this does not happen regularly?

         While admitting that there is no consensus, the authors provided three suggestions:

1. It does! This is the very reason that most extant dioecious plants are wind pollinated (Vamosi and Otto 2002).
2. Females counteract male negative adaptations quickly enough (Arnqvist and Rowe 2002).
3. Sexual selection may outweigh natural selection when an allele with a negative effect on fecundity becomes established in a population, because it is so sexually attractive (Muir and Howard, 1999). Extinction can ultimately occur. An example here might be the effect of transgene escape.

Regarding this third possibility, the authors present a model that illustrates the effect of such a trait that is beneficial to the male who is chosen because of it, but detrimental to the female that expresses it: a “sexual conflict”.

         Firstly two assumptions are made; that “haploid inheritance” is the mode of allele transfer to the next generation, and that an equal number of males as females survive. The trade off is that this allele “A” causes males to be more successful in mating (m) while at the same time reduces fecundity in females (f). Using mathematics to sort the permutations of fathers/mothers having/not having the gene, they found that this imaginary allele improved male mating success by 500%, while reducing female fecundity by 70% (m = 5, f = 0.3). If fecundity is below a certain level as A becomes established in the population, this is enough to bring the population to its knees (assuming nothing selects against the allele). The authors did note however, that in a population where the female does not suffer costs as a result of selecting her attractive male, she will, and thus the population will, benefit from strong sexual selection, especially when ‘parental care’ of offspring is part of the selection payoff: the chances for the next generation, and future generations are improved.

        Another aspect of sexual selection is the effect of female choice. This is in contrast to the above sexual conflict, where the female, the one in charge of fecundity, is often the ‘loser’ (Krebs and Davies 2004, p. 143). The establishment of resistance to a disease or parasite threat, for example, will occur more efficiently in a population if healthy males can demonstrate this state, thus allowing females to select them. This then, supports and expedites natural selection for the resistance gene. 

       Two established, but not necessarily conflicting, theories for mate selection are the Fisher and Zahavi hypotheses. Fisher showed how elaborate traits are selected for on the basis of attractiveness only. In the long tailed widow, for example (Krebs and Davies 2000 pp 190-196), long tails were initially selected for as the owners were better fliers. Ultimately, however, this selection led to birds whose tails were so long as to be a hindrance. Zahavi presented a ‘handicap’ hypothesis; the female chooses the showy male e.g. the peacock, as his current survival shows fitness and health despite his handicap. Brooks and Kokko mentioned these theories to illustrate how beneficial genes could be transmitted indirectly because of a sexually selected characteristic.

       Although female choice tends to select ‘better’ males (Houle and Koundrashov 2002), the cost of attractive traits in males may actually lead to lower male sexual success. This can mean that, on average, in a population where sexual selection is prominent, overall male viability might even be lowered.

        However, where strong sexual selection occurs, sexual dimorphism is seen. Selecting for bigger stronger males with large accoutrements, so they can win a mate, can mean selecting for individuals who consume a lot of resources….. The females of course need these resources for actual reproduction. So high male mortality may be beneficial when as a result, the females get more access to resources. High male mortality is seen (Promislow 1992, and others cited), and Kokko and Brooks present a second model to illustrate this potential benefit:

        Using a population of deer on an island, the investigators pit grass growth rate, g, (where total grass available is G), against consumption of grass by, and growth of, males and females (where males eat more). Fecundity is fixed but number of births is related to the number of females (F). Mortality and density dependence are linked, and male vulnerability (v) is taken into account. A process of mathematical differentiation lead the authors to show that there is a negative relationship between the stability of the whole population and, and how much more is eaten by the males, in comparison with the females. The more vulnerable (the higher the value of ‘v’) the males are in the equation, the more females can survive, and the greater the population size becomes overall.

         However according to this model, if vulnerability (v) is not increased along with male size in response to sexual selection, more males will survive to drain the resources, and both groups will suffer. It is precisely this scenario that the authors suggest, may have led to the demise of the Irish Elk (Megaloceros giganteus) around 10,000 years ago.

        The fact that sexual selection may not even have this effect of increasing male mortality in the first place, illustrates the problem in studying this area. It is difficult to prove the mutual exclusivity of one trait against another when there are so many variables and confounding factors, not including the false variables introduced by the statistical and study method (Krebs and Davies 2000, p 196). The authors acknowledged this; for each model and theory put forward, a potential alternative view was presented.

         The final two models refer to the case of the Irish Elk also. The authors highlight research that shows

-         large features such as antlers that make a male more attractive and so improve his mating success, can also cause him harm,

-         and that there can be positive or negative correlation between these large traits and viability.

      With this in mind, one model is based in a fixed environment, and fails to link extinction with sexual selection. However the extinction of the deer coincided with climatic change and the second model takes this into account.

          The simpler fixed model involved males that suffer because of their large antlers, but that the females suffer no cost. In a changing environment, those with smaller antlers might survive better, and thus meet more females. As males (competitors) with their expensive traits become fewer in number, the less well endowed males can now breed; previously they would not have been sexually selected. The result is a population more fit in the environment. In this situation extinction can only occur if the very few remaining large-antlered animals can breed with every female. The authors admitted that this would be unlikely.

         In a changing environment however, the situation is different. As a result of sexual selection, it is ‘assumed’ that the proportion of males with bigger antlers will increase during good breeding years. If this proportion is at 100% when a “catastrophe”[1] strikes, it was “assumed” that all large antlered males died. Extinction ensues.

        If the large-antlered males are less than 100%, and they are all wiped out, it was assumed that some lesser-antlered males survived. The authors suggested that the large antlers will only reappear as a result of mutation. If this mutation occurs, it will slowly be selected for, and in time gain a foothold once more. But only until the next catastrophe. Recurring catastrophes will keep the smaller-antlered males’ numbers high, and the population should persist. Very rare catastrophes are more detrimental, because they cripple the increasingly higher proportions of males that will have evolved large antlers.   Under all of these assumptions, the authors note that in a population where sexual selection is not utilised, the antlers remain small, and the model allows this population to survive, unlike the Elk.

        The authors did not suggest that sexual selection ‘from what was available’ could be the route to re-establish the vulnerable males with large antlers. An interesting confounding facet to this type of study is the phenomenon where males of some species can sometimes reduce their flamboyantly expensive traits in times of hardship.

         At present, there is some empirical evidence (with other species) to support this model….but also evidence to contradict it. The authors were left with many assumptions, too many unknowns, and these need further study in extant species, as well as retrospectively.

         

        The dynamics of sexual selection are not fully dealt with in this paper.  The maze of arguments would have been prohibitive! The authors do encourage specific further areas of study, particularly by examining the holes in their own models:

Ž    what are the demographic consequences of traits that are sexually selected but are detrimental for females?

Ž    is there a trade off between sexual selection and adaptations?

Ž    does sexual selection drive a population towards or away from extinction? Or both?

Ž    how is mate choice, including the effects of, and adaptations to, inbreeding, linked with the viability of a population?

Ž    what are the effects of hybridisation, and interspecies competion?

 

         The sturdiest rule of thumb to arise from this paper’s models is the following: sexual selection could result in extinction of a species, “evolutionary suicide”, if the negative effect of a trait is suffered by a different individual who enjoys the benefit.

 

Table 1: Summary of effects of sexual selection

Positive effects of sexual selection

Negative effects of sexual selection

* sexual selection has the effect of weeding out deleterious mutations if they adversely affect mating success     * it can speed up ‘evolution’ in response to a pressure e.g. as in the case of disease resistance       * attractive males can have ‘better’ genes to pass on

* male adaptations to improve mating success can lead to his downfall (conspicuousness, cumbersome ornaments, reduced disease resistance etc)   * it can produce traits so extreme that the population or species cannot adapt quickly enough to survive a disturbance e.g. climate changes     * extinction: males can pass on genes that have a negative effect when expressed in the females of the next generation, but the same genes benefited the reproductive success of the male. In essence, he who gains the benefit does not suffer the consequences himself.

 

 

References:

 

Darwin, C. 1859. On the origin of species. Reprinted 1985 Penguin Classics. P 131

 

Kokko and Brooks. (2003). Sexy to die for? Sexual selection and the risk of extinction. Ann. Zool. Fennici 40:207-219

 

Krebs and Davies, 2000. An introduction to behavioural ecology. Third ed. Blackwell Science. Pp

 

Krebs and Davies (eds), 2004. Behavioural ecology, An evolutionary approach. Fourth ed. Blackwell Science. Pp