Our model results indicate that in species with a strict social dominance hierarchy where social rank is determined by nepotism, a beneficial mutation occurring in a low-ranking female is not very likely to get established. This outcome emerged despite the immense advantage of the modeled mutation, which doubled its carrier’s survival probability. Moreover, the reproductive skew in our model (see Supplementary Fig. 1) was less radical than the skew reported for the spotted hyena females21, which means that in the model, low-ranking females had a relatively higher reproductive success potential than in reality. In other words, our model may be underestimating the severity of the negative selection a low rank induces.
It is reasonable to assume that a low-ranking mutant female in a female dominant society would produce very few surviving offspring due to her low rank and ensuing lack of access to resources. Thus, this female would have only a slight chance to transmit the mutation to the next generation. If this female does reproduce successfully and produces a female which also inherits the mutation, chances of this daughter to pass on the mutation are also slim, as her rank would be even lower than that of her mother. However, if the young produced is a male and has inherited the mutation, chances of transmitting the mutation may increase depending on the male’s reproduction odds. As demonstrated by the four scenarios, the reduction in mutation establishment with decreasing mutant female’s rank became more and more prominent with increasing restrictions on male reproduction. In all four scenarios, the mutation establishment rate median was zero for the lowest ranking mutants, and in all cases but Scenario I, it was <0.1 for at least the eight lowest ranking mutants (which represent 27% of females; Figs. 1 and 2). Yet, in Scenario I, where all males were equally likely to reproduce and die (except for mutants), the mutation had established rather well in many of the middle ranking mutants, with establishment rate median as high as 0.27 for the low rank of 23 (Fig. 1a). On the other end, in Scenario IV, establishment rate median values of above 0.25 are observed only for ranks of eight or higher, and even values just over 0.1 do not occur before the rank of 12 (Fig. 2b, Supplementary Table 1).
Thus, it follows that in species with female dominance over males and a strict female social hierarchy determined by nepotism, male selection scheme for reproduction may be crucial for the facilitation of a beneficial mutation establishment. Getting back to the spotted hyena, it is the second scenario that best describes this species social structure. In the spotted hyena males are ranked below females, but males’ rank affects only their priority of access to resources (which should affect survival, see21), whereas reproduction chances are independent of rank9,21,26,34. In fact, some females, particularly young ones, prefer lower-ranking immigrants, presumably to avoid inbreeding21,25,34. Since all immigrant males get to be new and low-ranking upon joining the clan, this behavior may be equivalent to giving an equal opportunity to all immigrant males. Indeed, Watts35 as well as Höner et al.26 found little reproductive skew among immigrant spotted hyena males. This may have two different consequences. On one hand, a male born to a low-ranking female may be less likely to survive due to low access to food in its natal clan and thus a rather poor physical condition upon dispersal, and for the same reason, it may have less chances to be admitted into a new clan26. In this case, the mutation would most likely be lost. On the other hand, a mutation may allow a migrating male of a low rank origin to better survive (in our model the mutation multiplied survival probability, a property which may be expressed in various ways, such as, for instance, better hunting capabilities), and thus the mutant male may be more likely to successfully join a new clan (either because its physical condition may permit more persistence upon encountering a new clan, or due to longevity which would facilitate extra search for clans). One way or another, it seems that the female preference for low-ranking males in the spotted hyena, not only serves to prevent inbreeding, as suggested by Höner et al.34, but also allows more gene flow and establishment of beneficial mutations, which otherwise would get lost.
Notably, the observed decreasing likelihood of mutation establishment along Scenarios I to III takes place in spite of complete independence between male choice and mutation presence. Male rank in these three scenarios either does not exist (Scenario I) or is defined merely by the order of joining a clan, which is independent of maternal rank or mutation presence. In the two first scenarios, mate choice by females is random. In Scenario III, male rank affects mate choice, but it is still completely independent of mutation presence or maternal rank. The observed diminishing establishment rate of the mutation stems, most likely, from the scarcity of the mutation when originating in a low-ranking female. As long as the mutation is rare, the probability of any single individual carrying it is low, and thus when a few males are more likely to survive and reproduce, the probability that this limited group of males carries the mutation would be further reduced compared to a larger group of potential mates.
The two mutations model further supports our conclusions. The fact that the median difference between the two mutations frequencies was negative in all four scenarios (Fig. 3) undoubtedly implies that a low rank constrains the establishment of a beneficial mutation. Moreover, the entire IQR, that is, 75% of the distribution of the difference in mutation establishment rate, rests in the negative region for Scenarios III and IV, and almost so for the first two scenarios. As in the single mutation models, the gradual increase in male reproduction restrictions along the four scenarios is reflected in a shift in location of both the median and the IQR of the mutations’ establishment rate difference.
Recent studies have examined the phenomenon of female dominance over males in a variety of species25,36,37,38,39. Some controversy has arisen regarding the definition of this term. Whereas the traditional definition of dominance examines the results of agonistic interactions and the evoking of submissive behavior25,36,37,40, later researchers suggest more subtle definitions such as priority of access to food and seasonal dominance which depends on energetic requirements at various life stages38,39,40. Thus, a variety of species, some of which rarely exhibiting agonistic interactions, or in which such interactions are not always decided one way or another, are included under this subtle definition of female dominance38,39,40. Yet, in most of these species, reproductive skew does not exist or was not reported. One major taxonomic group in which female dominance is the rule is the Lemuridae family, but reproductive skew is very low to nonexistent25,37,39. Other species in which some level of female dominance exists include the rock hyrax (Procavia capensis), rufous elephant shrew (Elephantus rufescens), velvet-furred swamp rat (Rattus lutreolus), brush-tailed possum (Trichosurus vulpecula), nutria (Myocastor coypus), Peruvian squirrel monkeys (Saimiri boliviensis peruviensis), Columbian ground squirrels (Spermophilus columbianus), snowshoe hares (Lepus americanus), Dall’s sheep (Ovis dalli), Angolan talapoin (Cercopithecus talapoin), rhesus macaque (Macaca mulata), tufted capuchin (cebus apella), bonobos (Pan paniscus), Garnett’s greater bushbabies (Otolemur garnettii), golden and Chinese hamsters (Mesocricetus, Cricetulus spp.), Maxwell’s duikers (Cephalophus maxwelli), otters (Amblonyx cinerea, Lutrogale perspicilla), and beavers (Castor canadensis)25,36,38,39,<a data-track="click" data-track-action="reference anchor" data-track-label="link" data-test="citation-ref" aria-label="Reference 41" title="Boinski, S. The social organizations of squirrel monkeys: implications for ecological models of social evolution. Evol. Anthropol. 8, 101e112;
https://doi.org/10.1002/(SICI)1520-6505(1999)8:33.0.CO;2-O
(1999).” href=”https://www.nature.com/articles/s42003-022-03901-z#ref-CR41″ id=”ref-link-section-d14227943e908″>41. Although female dominance hierarchy exists in a few of these species (e.g., Peruvian squirrel monkey<a data-track="click" data-track-action="reference anchor" data-track-label="link" data-test="citation-ref" aria-label="Reference 41" title="Boinski, S. The social organizations of squirrel monkeys: implications for ecological models of social evolution. Evol. Anthropol. 8, 101e112;
https://doi.org/10.1002/(SICI)1520-6505(1999)8:33.0.CO;2-O
(1999).” href=”https://www.nature.com/articles/s42003-022-03901-z#ref-CR41″ id=”ref-link-section-d14227943e912″>41, ring-tailed lemur (Lemur catta)39,42, Verreaux’s sifaka (Propithecus verreauxi))13,25, we did not find any studies indicating female reproductive skew in any of them. Holekamp and Engh25, who reviewed the more classical female dominant species, also reported no evidence for female reproductive skew.
This seemingly lack of female reproductive skew among most female dominant species is quite surprising in light of the rather common correlation between social rank and female reproductive success in male dominant species. To mention a few, considerable female reproductive skew is found in baboons (Papio spp), macaques (macaca spp.), feral horses (Equus caballus) and plains zebras (Equus burchelli)8,15,19.
Holekamp and Smale28 state that “reproductive skew among female spotted hyenas appears to be greater than that documented among females of male-dominated species characterized by plural breeding”. They suggest that the key determinant of reproductive success among females in this species is rank-related priority of access to food resources. This high priority is reinforced by female dominance over males and is particularly important as this species resides in an environment in which prey availability is seasonal and scarce at times21. Our study suggests that this extreme difference in reproductive success, which, unlike in male-dominated species, is determined by nepotism rather than by physical characters, may induce a handicap on the entire population preventing the establishment of beneficial mutations. This may also hinder adaptation to a changing environment. However, our study results indicate that male equal access to females may, at least partially, counter the inhibition effect on a beneficial mutation establishment. More research is necessary in order to investigate female reproductive skew in species with a social structure similar to that of the spotted hyena, which is characterized by female dominance over males, plural breeding, and a strict female linear social hierarchy determined by nepotism.
One intriguing possibility for testing this model’s validity would be an empirical study, provided that the value of some adaptive trait can be measured. In the case of the spotted hyena such a trait may refer to hunting success or physical capabilities. It is well established that adult female spotted hyenas are larger and more aggressive than adult males21, but little attention has been allocated to the study of individual physical differences among females of different ranks. Smith et al.43 studied within clan aggression in the context of the fission-fusion behavior characterizing the spotted hyena clans. Their results indicate more frequent aggression and resulting fissions occurring during times of food shortage. Rank was found to be the major correlate of an aggressive incident result. If it is possible to identify low-ranking females with some beneficial trait (independent of rank), it would be interesting to follow such females’ inclusive reproductive success along time, and even more so, the reproductive success of their sons.
Another possible path around the conflict this model suggests would be through the selection of male admission into new clans. Male admission into clans is often constrained by severe aggression of resident immigrant males which may prevent or delay male admission21,26. Such behavior may in fact promote mutant male chances, at least in the case of a mutation that improves physical capabilities.
One last, though not very likely possible detour around this difficulty is the occurrence of dominance rank exchanges. Such rank improvements are not very common among female dominated societies, except for in the case of aging females who may clear the way for their daughters44. However, Straus and Holekamp44 found that individuals who repeatedly form coalitions with their top allies are likely to improve their position, and, according to Strauss and Holekamp44, “facilitate revolutionary social change”. It should be kept in mind that not only are such incidents rather rare, but they are unlikely to turn a very low-ranking female into a high-ranking one, especially not when group size is large.
More empirical and theoretical research should shed more light on this intriguing question of possible maladaptive evolution. Our model, in line with a few other models such as that of Holman31, suggests that evolution may not always lead to the best solution. As in every process, a local optimum may get evolution trapped and prevent further advance to better optima.
Source: Ecology - nature.com
