Sexual selection has been increasingly acknowledged as a major evolutionary driver in many taxa. An unequal mating success arising through competition over mates is the phenomenon that defines sexual selection. Therefore, demonstrating the presence of sexual selection requires that the number or quality of mates are spread less evenly than random processes would suggest. The objective of this study was to estimate the extent of this inequality in male mammals by reviewing studies that measure variance in genetic paternity. I found that few species showed high values of the standardised variances in male reproductive success, Im, and Nonacs´s B indices. These species differed from those with low or medium values in that, while in the latter the females breed solitary, in the former, they are grouped for reproduction, which possibly facilitates mate monopolization by males. Low levels of variance in reproductive success could be explained because most species of mammals breed solitary or due to high rates of extra-pair copulations by ‘subordinate’ males.Fil: Cassini, Marcelo Hernan. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Biología y Medicina Experimental. Fundación de Instituto de Biología y Medicina Experimental. Instituto de Biología y Medicina Experimental; Argentin

Cassini, Marcelo Hernan

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Published by Associazione Teriologica Italiana Volume 33 (2): 123–125, 2022Hystrix, the Italian Journal of MammalogyAvailable online at:http://www.italian-journal-of-mammalogy.it doi:10.4404/hystrix–00483-2021CommentaryMeasuring sexual selection in mammalsMarcelo H. Cassini∗Laboratorio de Biología del Comportamiento, Instituto de Biología y Medicina Experimental, Obligado 2490, 1428 Buenos Aires, ArgentinaKeywords:evolutionpaternitygenetic reproductive successbreeding systemmating systemArticle history:Received: 16 August 2021Accepted: 06 October 2022AcknowledgementsI want to thank to Dr D. Lukas for gently provided me with databasesof his work and to Dr. Nonacs for his advice in the use of his index.AbstractSexual selection has been increasingly acknowledged as a major evolutionary driver in many taxa.An unequal mating success arising through competition over mates is the phenomenon that definessexual selection. Therefore, demonstrating the presence of sexual selection requires that the numberor quality of mates are spread less evenly than random processes would suggest. The objectiveof this study was to estimate the extent of this inequality in male mammals by reviewing studiesthat measure variance in genetic paternity. I found that few species showed high values of thestandardised variances in male reproductive success, 𝐼𝑚, and Nonacs’s 𝐵 indices. These speciesdiffered from those with low or medium values in that, while in the latter the females breed solitary,in the former, they are grouped for reproduction, which possibly facilitates mate monopolization bymales. Low levels of variance in reproductive success could be explained because most species ofmammals breed solitary or due to high rates of extra-pair copulations by “subordinate” males.IntroductionSexual selection is considered one of the most pervasive forces thatdrive the evolution of reproductive traits in sexually reproducing or-ganisms (Andersson, 1994). Darwin (1871) defined sexual selectionas being dependent “on the advantage which certain individuals haveover other individuals of the same sex and species, in exclusive relationto reproduction" (p. 871). A modern definition proposes that sexual se-lection favours investment in traits that improve the likelihood of fertil-ization given limited access to opposite-sex gametes due to competitionwith members of the same sex (Jennions and Kokko, 2010).Sexual se-lection should be particularly intense in mammals because females bearmost parental investment due to gestation and lactation, transformingthem in a limiting resource for which males compete (Trivers, 1971).An unequal mating success that arises through competition overmates is the phenomenon that defines sexual selection (Arnold andWade, 1984). Therefore, demonstrating the presence of sexual se-lection requires that the number or quality of mates are spread lessevenly than random processes would suggest, in at least one of the sexes(Kokko and Jennions, 2008). Kokko et al. (1999) [p. 358] stated that,“unless the inequality itself can be shown to exist, and preferably meas-ured and tested for significance, any further study of the causes behindit is fruitless”.In order to measure variance in mating success, a type of sexual se-lection index must be selected and the data that this type of index re-quires must be obtained. In the literature, there is a several indices(Klug et al., 2010; Anthes et al., 2017). Nevertheless, most indices cor-relate very strongly and measuring the same data with multiple indiceswill rarely reveal novel insights (Nonacs, 2003). In this paper, I usedthe variance in relative reproductive success, the so called intensity (oropportunity) of sexual selection on males 𝐼𝑚, which is calculated as thevariance divided by the square of the mean (Arnold and Wade, 1984).I used 𝐼𝑚 because it is the most common index used in mammalian lit-∗Corresponding authorEmail address: mhcassini@yahoo.com.ar (Marcelo H. Cassini)erature (Isvaran and Sankaran, 2017). Based on the range shown formammalian species, (Dubuc et al., 2014) I considered values of 𝐼𝑚<1to show weak opportunity for selection, values between 1 and 3 to showmoderate opportunity, and values of 𝐼𝑚>3 to show high opportunity forselection.Ideally, data to measure sexual selection should be generated with anexperimental design that includes the entire reproductive period (Fritz-sche and Booksmythe, 2013), because experiments can assess causalrelationships (Anthes et al., 2017). Clearly, this type of experiment isimpossible to conduct with most mammals. Thus, most of the clas-sical studies in this taxon were conducted using behavioural traits thatare indirectly related to reproductive success, e.g. harem size (Em-len and Oring, 1977). Using these behavioural surrogates, the over-all result was that mammals showed high skew in reproductive suc-cess (review, for example, in Clutton-Brock, 1988). Recently, thesemeasures have been replaced by estimations of paternity using genetictechniques, which provides a valuable measure of the opportunity ofsexual selection because it excludes the possibility that males who arenot dominant in direct competition for mates may obtain extra-groupcopulations (Wade and Shuster, 2004).The objectives of this work were: (i) to review the literature on ge-netic paternity in mammals in order (ii) to obtain estimates of the op-portunity of sexual selection in this taxon, (iii) to compare genetic withbehavioural measures of male reproductive success and (iv) to discussthe role of sexual selection in mammalian evolution.MethodsCreating datasetsFor paternity data, the methodology of Isvaran and Sankaran (2017)was adopted which aimed to isolate estimates of access to fertilization(i.e., the effect of sexual selection on variation in reproductive success)and remove the effect of factors related to viability selection (i.e., sur-vival between breeding seasons and lifespan). A literature search wasconducted for estimates of male genetic mating success, based on ge-Hystrix, the Italian Journal of Mammalogy ISSN 1825-5272 20th December 2022©cbe2022 Associazione Teriologica Italianadoi:10.4404/hystrix–00483-2021Hystrix, It. J. Mamm. (2022) 33(2): 123–125netic measures of paternity (Supplemental Table S1). This search hadfour stages. In the first, I used two keywords in Google Scholar data-base, “paternity” and “mammal”, to get a first list of articles. Thesecond stage consisted of a review of those journals that appeared inthe first stage, using the same two words in the search tools available inthe web pages of the journals themselves. The third stage consisted ofa review of the literature cited in all the articles obtained in the secondstage. The fourth stage consisted of a review of the literature cited inall the articles obtained in the third stage. Only fieldwork studies wereconsidered unless otherwise mentioned.In order to obtain a measure of inequality in reproductive success, itwas necessary to extract the information on paternity from each study.In all studies, paternity was established through the use of molecularmarkers and, in order to do so, skin or blood samples were taken fromthose parents and offspring that were captured and then the degree ofkinship was determined. In most cases, male reproductive success waspresented as the number of pups that were assigned to each sampledmale. Therefore, I calculated the variance and the mean in male repro-ductive success of the total of the sampled males. In some cases, thevariance and the mean were directly provided by the study. In studiesthat report male reproductive measures counted across multiple years,the annual mean number of offspring per male was obtained first, tothen obtain the mean and variance for the total number of males.Female breeding system data were obtained from Lukas andClutton-Brock (2013). Information gaps were filled with informationprovided by the Animal Diversity Web, University of Michigan (https://animaldiversity.org/ accessed September-November 2020). Data onmating systems were obtained from the same sources of paternity data.Measuring inequality in reproductive successI used the “opportunity of sexual selection” calculated as 𝐼𝑚 = 𝑣𝑎𝑟𝑚𝑒𝑎𝑛2of paternity data. I followed Dubuc et al. (2014) criteria to define low,medium and high skew in male reproductive success. Complementingand for comparison, I calculated the Nonacs’ 𝐵 index (Nonacs, 2000,2003) using the program Skew Calculator 2003 (http://www.eeb.ucla.edu/Faculty/Nonacs/PI.html), which tests whether paternity distributionis different from that expected by chance. This program allows split-ting into separate groups, but I did not so because only a few numberof studies provided data by group. This program provides the follow-ing confidence intervals of 𝐵: (i) if they include zero, the distributionof benefits is not different from random chance; (ii) if the lower confid-ence interval includes the “equal sharing” value (also provided), thenan equal distribution of benefits cannot be excluded; (iii) if the intervalsdo not include zero, this indicates a skew distribution of paternity, withsome males being significantly more successful than others; (iv) un-der the conditions of (iii), 𝐵 values close to zero indicate low variancein mating success, while 𝐵 values close to one indicates high levels ofpaternity monopolisation. Therefore, values <0.5 were considered lowskew values, and >0.5 were considered high. I included studies thatboth sampled and not sampled unsuccessful males. This could affectthe level of skew estimated with 𝐼𝑚 but is more controlled by 𝐵.Relating variablesAll relationships were analysed employing the phylogenetic generalisedleast squares (PGLS) method in R, so the phylogenetic signal couldbe controlled Martins and Hansen (1997). First, a simple regressionwas conducted to compare 𝐼𝑚 with 𝐵, then a multiple regression wasconducted with 𝐼𝑚 as a dependent variable (log transformed, with fivezero-data assigned a value of −2) and four independent variables: bodysize (log transformed), sexual size dimorphism (log transformed) andtwo proxy measures of strength of sexual selection, based on the in-tensity of the male competition for mates: mating system (polygyny,polygynandry, monogamy) and female breeding system (plural versussingle breeders).Figure 1 – Percentages of low, moderate and high values of standardised variance in malereproductive success was calculated: 𝐼𝑚 and Nonacs’ 𝐵 index. Low values of opportunityof sexual selection were significantly more frequent than high values.ResultsA dataset was built containing genetic variance information from a totalof 158 mammal species, of which 156 had data that allowed the es-timation of 𝐼𝑚, and 126 had data that allowed the estimation of 𝐵.Mean 𝐼𝑚 and 𝐵 were 1.48 (s.d.=2.04) and 0.027 (s.d.=0.098). As ex-pected, 𝐼𝑚 and 𝐵 were strongly correlated (_=0, 𝑟2=0.22, 𝐹1,116=33.8,p<0.001). According to the categorisation made by Dubuc et al. (2014),most species showed weak selection opportunity (50.3%), while only13.8% of species had high levels of selection opportunity and 35.8 %showed a moderate opportunity for sexual selection (Fig. 1). These fre-quencies showed statistically significant differences (𝜒2=32.2, d.f.=21,p<0.001). The 𝐵 index showed a similar pattern (Fig. 1), given thatthe number of species with non-skewed (equal or random) distribu-tions (59.1%) was higher than the number of species with a skewness(𝜒2=4.2, d.f.=1, p=0.04).Four behavioural measures of sexual selection were compared with𝐼𝑚 (Tab. 1). The only significant correlation was between 𝐼𝑚 and thebreeding system.Table 1 – Results of the phylogenetic generalised least squares using standardised variancein male reproductive success 𝐼𝑚 as dependent variable and four independent variables:breeding and mating systems. The global analysis gave: _=0, 𝑟2=0.08, 𝐹1,133=2.94,p=0.02.Independentvariable Estimate Std. Error t-value p-value(Intercept) −0.45 0.15 −30.80 0.0002Body mass 0.01 0.04 0.14 0.89Sexual dimorphism 0.43 0.40 1.06 0.29Breeding system 0.33 0.11 29.40 0.003Mating system 0.02 0.04 0.64 0.52DiscussionResults obtained in this study, which used the largest available data-set on genetic measures of paternity variance in mammals, suggest lowlevels of opportunity of sexual selection in this taxon. A possible ex-planation of these low values of genetic measures of variance in repro-ductive success would be the effect of extra-group copulations. Mostmammalian species were described as behaviourally polygynous, withconsequent variance in the ability of males to monopolize females (Em-len and Oring, 1977). Large males can monopolise females by contestcompetition, while small males can evolve alternative reproductive tac-tics, such as sneak spawning (Jennions and Kokko, 2010). If extra-paircopulations are achieved by less successful males in direct competition,the result is a decrease in the variance in male reproductive success.In populations with more than one type of male reproductive tactic, it124Measuring sexual selection in mammalscould be that ethological observations indicate a high variance in repro-ductive success with large males gaining more mates that small ones,but this does not necessarily imply a high paternity variance, since al-ternative tactics could be equally effective but less conspicuous, withthe consequent homogenization of this variable. Under this hypothesis,sexual selection operates maintaining equilibrium between two or morealternative reproductive strategies depending on their size or age.This hypothesis was partially tested by Isvaran and Sankaran (2017),who showed that when breeding group sex ratios are strongly female-biased (highly polygynous systems, multi-male systems with female-biased groups), extra-group paternities appear to decrease variance inmale reproductive success. These authors described this result as ’anunsuspected relationship between overt (social mating system) and cov-ert (extra-group paternity) mating tactics and the potential for sexualselection in male mammals’.A correlation between breeding system and intensity of sexual se-lection was found. This relationship is predicted by sexual selectiontheory, which postulates that the extent to which breeding females ag-gregate affects mating competition (Emlen and Oring, 1977). In pluralbreeding species, the number of potential breeding partners that in-dividual males can guard effectively is higher than in singular breed-ers, increasing variance in male reproductive success (Kvarnemo andAhnesjo, 1996). In most mammalian species, females breed solitary(Lukas and Clutton-Brock, 2013), therefore it is expected relatively lowlevels of intensity of sexual selection in this taxon if sexual selection in-creases with female group size.Another hypothesis is that current variation in reproductive successrefers only to the maintenance of sexually selected traits, not their ori-gin and further evolution in the past, when variance in reproductive suc-cess might have been different (Grafen, 1988). In other words, the traitwould cause skewed reproduction among males, but would quickly be-come fixed (Fisher’s run-away model of sexual selection, Fisher, 1930).This study only analyses the current opportunity of sexual selectionmeasured as variance in parenting but does not say anything about theimpact of sexual selection on actual traits, such as sexual size dimorph-ism. Those traits need to be heritable and have strong enough fitnessadvantages to show change in trait forms over evolutionary time. There-fore, a future study should analyse the relationship between sexual traitsand paternity variance in mammals.ReferencesAndersson M., 1994. Sexual selection. Princeton University Press, New York.Anthes N., Häderer I.K., Michiels N.K., Janicke T., 2017. Measuring and interpreting sexualselection metrics: evaluation and guidelines. Methods in Ecology and Evolution 8(8):918–931.Arnold S.J., Wade M.J., 1984. On the measurement of natural and sexual selection: applic-ations. Evolution 38(4): 720–734. doi:10.2307/2408384Clutton-Brock T.H. (Ed.), 1988. Reproductive success: studies of individual variation incontrasting breeding systems. University of Chicago Press, Chicago, IL.Darwin C., 1871. The Descent of Man, and Selection in Relation to Sex. John, London,UK.Dubuc C., Ruiz-Lambides A., Widdig A., 2014. Variance in male lifetime reproductivesuccess and estimation of the degree of polygyny in a primate. Behavioral Ecology 25(4):878–889.Emlen S.T., Oring L.W., 1977. Ecology, sexual selection and the evolution of mating sys-tems. Science 197: 215–223.Fisher R.A., 1930. The genetical theory of natural selection, 1st ed. Clarendon Press, Ox-ford, U.K.Fritzsche K., Booksmythe I., 2013. The measurement of sexual selection on females andmales. Current Zoology 59(4): 558–563.Grafen A.T.H., 1988. On the Uses of Data on Lifetime Reproductive Success. In: Clutton-Brock T.H. (Ed.) Reproductive success: studies of individual variation in contrastingbreeding systems. University of Chicago Press, Chicago, IL.Isvaran K., Sankaran S, 2017. Do extra-group fertilizations increase the potential for sexualselection in male mammals? Biology Letters 13: 283–295.Jennions M., Kokko H., 2010. Sexual Selection. In: Westeat J., Fox M. (Eds.) EvolutionaryBehavioral Ecology. Oxford University Press, Oxford, U.K.Kvarnemo C., Ahnesjo I., 1996. The dynamics of operational sex ratios and competitionfor mates. Trends in Ecology and Evolution 11(10): 404–408.Klug H., Heuschele J., Jennions M.D., Kokko H., 2010. The mismeasurement of sexualselection. J. Evol. Biol. 23: 447–462.Kokko H., Mackenzie A., Reynolds J.D., Lindström J., Sutherland W.J., 1999. Measures ofinequality are not equal. The American Naturalist 154(3): 358–382.Kokko H., Jennions M.D., 2008. Parental investment, sexual selection and sex ratios.Journal of Evolutionary Biology 21(4): 919–948.Lukas D., Clutton-Brock T.H., 2013. The evolution of social monogamy in mammals. Sci-ence 341(6145): 526–530.Martins E.P., Hansen T.F., 1997. Phylogenies and the comparative method: a general ap-proach to incorporating phylogenetic information into the analysis of interspecific data.The American Naturalist 149(4): 646–667.Nonacs P., 2000. Measuring and using skew in the study of social behavior and evolution.Am. Nat. 156: 577–589.Nonacs P., 2003. Measuring the reliability of skew indices: is there one best index? Anim.Behav. 65: 615–627.Trivers R. L., 1971. The evolution of reciprocal altruism. Quarterly Review of Biology 46:35–57.Wade M.J., Shuster S.M., 2004. Sexual selection: harem size and the variance in malereproductive success. The American Naturalist 164(4): E83–E89.Associate Editor: R. ChirichellaSupplemental informationAdditional Supplemental Information may be found in the online version of this arti-cle:Table S1 Literature search results.125

Measuring sexual selection in mammals

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Measuring sexual selection in mammals

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