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Monotocy and the evolution of plural breeding in mammals

Monotocy and the evolution of plural breeding in mammals Downloaded from https://academic.oup.com/beheco/article/31/4/943/5830852 by DeepDyve user on 12 July 2022 applyparastyle "fig//caption/p[1]" parastyle "FigCapt" The official journal of the Behavioral ISBE Ecology International Society for Behavioral Ecology Behavioral Ecology (2020), 31(4), 943–949. doi:10.1093/beheco/araa039 Original Article Monotocy and the evolution of plural breeding in mammals a,b, a Dieter Lukas and Tim Clutton-Brock Department of Zoology, University of Cambridge, Downing Street, CB2 3EJ Cambridge, UK and Department of Human Behavior, Ecology and Culture, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103 Leipzig, Germany Received 7 August 2019; revised 6 March 2020; editorial decision 3 April 2020; accepted 14 April 2020. In many mammals, breeding females are intolerant of each other and seldom associate closely but, in some, they aggregate in groups that vary in size, stability, and kinship structure. Aggregation frequently increases competition for food, and interspecific differences in female sociality among mammals are commonly attributed to contrasts in ecological parameters, including variation in activity timing, the distribution of resources, as well as the risk of predation. However, there is increasing indication that differences in female soci- ality are also associated with phylogenetic relationships and with contrasts in life-history parameters. We show here that evolutionary transitions from systems where breeding females usually occupy separate ranges (“singular breeding”) to systems where breeding females usually aggregate (“plural breeding”) have occurred more frequently in monotocous lineages where females produce single young than in polytocous ones where they produce litters. A likely explanation of this association is that competition between breeding females for resources is reduced where they produce single young and is more intense where they produce litters. Our findings rein- force evidence that variation in life-history parameters plays an important role in shaping the evolution of social behavior. Key words: life history, social competition, sociality, phylogenetic reconstruction. INTRODUCTION these systems predominate within some Orders, including ungu- lates, cetaceans, and primates (Clutton-Brock 2016; Ward and In many mammals, adult females compete for access to resources Webster 2016). In most “plural breeders,” groups usually consist necessary to raise young and occupy separate ranges or territo- of breeding females born in the same group, as well as a number ries during the breeding season—as in many rodents, insectivores, of nonbreeding natal males that will eventually disperse to breed and nocturnal carnivores (Eisenberg 1983; Wolff and Sherman elsewhere, together with one or more immigrant males that fa- 2007; Clutton-Brock 2016). The ranges of breeding females in ther most of the young born in the group. In a small number of these “singular breeders” overlap to varying extents with those of species, groups consist of immigrant breeding females together neighboring females, as well as with those of males: in some, fe- with one or more natal breeding males (Clutton-Brock 1989; males defend exclusive territories against members of both sexes, Lukas and Clutton-Brock 2011). Intraspecific variation in group whereas, in others, they share their territories with particular males size is common (Richard 1974; Lott 1991) and, in some cases, but exclude other mature females; in some, there is extensive range groups in some populations usually contain multiple breeding fe- overlap between neighboring females, whereas, in others, breeding males, whereas, in others, many contain a single breeding female females share their ranges with nonbreeding relatives and unrelated (Schradin 2013). In many cases, this variation appears to reflect breeding males but forage separately; finally, in a few, breeding fe- contrasts in population density, with larger numbers of breeding males associate with nonbreeding relatives of both  sexes in cohe- females in groups where population densities are higher. sive groups as in the social mole-rats and some social mongooses Many comparative studies have explored the distribution of (Jarvis 1981; Clutton-Brock 2016). female group size in particular Orders of mammals and have In other species, breeding females are more tolerant of each shown that interspecific differences are related to variation in other and multiple breeding females share a common range and habitat use, feeding ecology, activity timing, and population den- form groups that include multiple individuals that breed regularly sity (Jarman 1974; Kaufmann 1974; Bradbury and Vehrencamp (Lewis and Pusey 1997; Clutton-Brock 2016). Although a rela- 1977; Clutton-Brock and Harvey 1977; Gittleman 1989; Wright tively small proportion of all mammals form groups of this kind, 1999; Fisher and Owens 2000; Ebensperger 2001), as well as to contrasts in body size, longevity, litter size, and juvenile develop- Address correspondence to D. Lukas. E-mail: [email protected] ment (Eisenberg 1983; van Schaik and Kappeler 1993; Rubenstein © The Author(s) 2020. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. Downloaded from https://academic.oup.com/beheco/article/31/4/943/5830852 by DeepDyve user on 12 July 2022 Behavioral Ecology and Abbot 2017; Smith et al. 2017). However, analyses of variation Here, we use comparative data for mammals and phylogenetic in female sociality seldom distinguish between groups that incor- reconstructions to investigate whether there is a consistent rela- porate several breeding females (plural breeders) and groups that tionship between the evolution of monotocy and the distribution include a single breeding female (singular breeders). The distinc- of plural breeding. Given that plural breeding is rarer and ap- tion between total group size and the number of breeding females parently the derived system, we investigated whether contem- that aggregate is important for it is the extent to which breeding porary mammals in which plural breeding has been observed at females aggregate that affects social and mating competition. When all are more likely to be monotocous, whereas species in which breeding females aggregate, the number of potential breeding part- only singular breeding occurs are more likely to be polytocous. ners that individual males can guard effectively is higher (Emlen To test the prediction that transitions to the production of single and Oring 1977), potentially increasing the intensity of sexual se- offspring remove constraints on aggregation in breeding females, lection on males (Kvarnemo and Ahnesjo 1996) and the extent we subsequently investigated whether any transitions to plural to which breeding males aggregate with each other (Andelman breeding have been more common in monotocous lineages than 1986). The number of breeding females in a group also affects so- in polytocous ones. cial interactions by influencing average levels of kinship between group members (Lukas et al. 2005; Lukas and Clutton-Brock 2018). Although contrasts in group size often reflect differences in the MATERIAL AND  METHODS number of breeding females that associate with each other, the re- Data and classifications lationship between total group size and the number of breeding females per group is inconsistent (Rubenstein et  al. 2016). For ex- We based the classification of the social system of mammals on our ample, some of the largest stable social groups found in mammals previous databases (Lukas and Clutton-Brock 2013, 2017a) and ex- occur in singular breeders, like naked mole-rats (Heterocephalus glaber) cluded the few mammalian species in which females produce eggs. where colonies can include several hundred individuals but only a We identified species as monotocous if median litter size was less single female breed in each group (Jarvis 1981; Braude 2000). than 1.5 and as polytocous if it was greater than 1.5. Data for litter Previous theories about the evolution of sociality among size (number of young per birth, central tendency across females in breeding females (plural breeding) have focused on its association wild populations), for adult body mass (female mass in grams, cen- with diurnal activity patterns and susceptibility to predation, as well tral tendency across females in both captive and wild populations), as with reliance on resources where direct competition between in- for diurnality (whether a species is strictly nocturnal or whether dividuals foraging in close proximity is not intense (Jarman 1974; part of its activity occurs during the day), and for diet (whether a Wrangham 1980). However, there are both theoretical and empir- species is a herbivore, carnivore, or omnivore) were obtained from ical reasons for expecting life-history parameters to also play an a combination of primary and secondary sources, including pub- important role. Lactating females experience substantial increases lished databases (Carey and Judge 2002; Ernest 2003; Bielby et al. in energetic requirements in all mammals and the energetic costs 2007; McCarthy et al. 2008; de Magalhaes and Costa 2009; Jones of raising young increase with litter size (Speakman 2008; Hamel et  al. 2009; Wilman et  al. 2014). If entries in these databases dif- et al. 2010; Hinde and Milligan 2011). As a result, competition be- fered slightly, we used the median value and, if entries were sub- tween coresident breeding females for resources necessary to raise stantially different, we referred to the primary literature to identify offspring is likely to be more intense in polytocous species (where the most likely value. females produce multiple young at once) than in monotocous ones We restricted species in our analysis to those for which field- (females produce single young). Comparative studies support this: based reports of social behavior were available (following Schradin for example, female infanticide appears to be more frequent in 2017; Lukas and Clutton-Brock 2017b). We identified species as polytocous than monotocous species (Lukas and Huchard 2019). In singular breeders if most females occupy separate home ranges addition, polytocy is usually associated with the production of rela- or territories during the breeding season (even if they share these tively altricial infants that need to be maintained in a nest or burrow with nonbreeding females or with males) and as plural breeders if (Eisenberg 1983; van Schaik and Kappeler 1993). As a result, many multiple breeding females share a common range and actively as- polytocous mammals are central place foragers (Stephens and sociate with each other (Ward and Webster 2016), forming groups Krebs 1986), which increases the energetic costs of aggregation in that usually include more than one individual that breeds regu- breeding females and so may constrain the evolution of sociality larly. Our definition of plural breeding includes fission–fusion spe- in breeding females (Kappeler 1998). Phylogenetic comparisons cies, such as chimpanzees where females may spend part of the also suggest that monotocy may facilitate the evolution of soci- day foraging independently but live in discrete communities that ality. Although singular breeding and polytocy appear to have been include multiple breeding females that share a common range. We the ancestral condition in many phylogenetic groups of mammals classified species that live in mixed sex pairs or in groups where (Leutenegger 1979; Lukas and Clutton-Brock 2013; Werneburg only a single female breeds regularly (like the social mole-rats, et  al. 2016), many of the mammalian taxa where plural breeding callitrichid primates, and several social mongooses) as singular is common are monotocous—including the primates, ungulates, breeders. We focus our classification of sociality on the behavior and cetaceans (Eisenberg 1983; Clutton-Brock 2016). Transitions to of breeding females, those that are in the later stages of preg- monotocy from polytocy appear to be rare and to have occurred at nancy or have dependent young and do not consider the beha- a relatively early stage in many mammalian lineages (Leutenegger vior of juveniles, males, or adult females who are not breeding. 1979; Bordes et  al. 2011; Werneburg et  al. 2016; Battistella et  al. In some species where breeding females commonly aggregate, 2019), whereas transitions in sociality appear to be more recent some breeding groups include a single breeding female, whereas (Blomberg et al. 2003; Kamilar and Cooper 2013), suggesting that others include several females that breed regularly (Nievergelt transitions to monotocy in these mammalian lineages might have et al. 2002; Dalerum 2007; Schradin et al. 2012; Weidt et al. 2014; removed constraints on the evolution of plural breeding. Valomy et al. 2015; Agnani et al. 2018; Miles et al. 2019). Where Downloaded from https://academic.oup.com/beheco/article/31/4/943/5830852 by DeepDyve user on 12 July 2022 Lukas and Clutton-Brock • Monotocy and female sociality in mammals intrapopulation variation of this kind was reported, we classified RESULTS species as plural breeders if, throughout the breeding season, most In the 1267 species in our sample, 44% were classified as breeding females are found in groups where several females breed monotocous and 56% as polytocous. In 54% of the mamma- regularly and as singular breeders if the majority of breeding fe- lian Orders represented in our sample, all species were either males were found in groups that included a single breeding female. monotocous or polytocous, whereas 46% of Orders included We used a majority rule to reduce risks of misclassification of rare both monotocous and polytocous species. Polytocy is predominant observations that are likely to be nonadaptive (following Schradin (more than 75%) in 10 of the 24 mammalian Orders represented et  al. 2018). In the small number of species where studies of dif- in our sample, whereas monotocy predominates in another 10 (see ferent populations have shown that plural breeding predominates Figure 1). in some populations or at some times, whereas singular breeding Although 56% of contemporary mammals in our sample predominates in others, often in association with relatively low are polytocous, more than 85% of all species classified as plural population density (e.g., striped mice; Schradin et  al. 2012), we breeders in our sample are monotocous and, in all seven Orders of classify them as plural breeders if plural breeding predominates mammals where plural breeding is common (artiodactyls, cetaceans, in either population as this is the rarer and derived system. It bats, diprotodons, perissodactyls, proboscidea, and primates), most has been suggested that, where multiple records of female group or all species are monotocous (see Figure  1). Compared with spe- size are available, they should be included as separate points (e.g. cies that we classified as singular breeders (and controlling for Miles et  al. 2019). However, like most other comparative studies, phylogenetic effects), plural breeding mammals have significantly we preferred to include a single value for each species in order smaller litter sizes (mean effect of larger litter size: −118.0, 95% to avoid particular species weighting our analyses disproportion- CI: −168.7 to −76.5; 810 singular vs. 457 plural breeders): among ately. We also generally do not have matching data on litter size singular breeders, median litter size is 3 and more than 80% of spe- for each population, so we cannot attempt to explain the full var- cies produce two or more offspring per breeding attempt. In con- iation in sociality across populations; we do not know the history trast, among species classified as plural breeders, median litter size of the populations within a given species, so we cannot infer if and is one and only 14% of species produce two or more offspring per how often transitions in sociality might have occurred (Stone et al. breeding attempt. 2011). The number of species for which multiple records showing The influence of litter size on the distribution of plural breeding differences in female sociality are available is relatively low and is independent of whether a species is nocturnal or diurnal (effect whether they are classified as plural or singular breeding does not of larger litter size on occurrence of plural breeding: −25.4, 95% appear to affect the outcome of our analyses. CI: −33.1 to −16.5; effect of being nocturnal rather than diurnal: For our phylogenetic reconstructions, we relied on a mamma- −8.9, 95% CI: −13.2 to −4.7; 374 singular vs. 115 plural breeders) lian supertree (Rolland et al. 2014) and did not resolve polytomies and whether it is omnivorous, herbivorous, or carnivorous (effect or modify the branch lengths in any analyses. All data and sources of larger litter size on occurrence of plural breeding: −19.7, 95% are deposited at the Knowledge Network for Biocomplexity (doi: CI: −27.8 to −11.4; effect of being herbivore rather than carnivore 10.5063/F1P8497S). or omnivore: 7.7, 95% CI: 0.5 to 15.7; 409 singular vs. 333 plural breeders). In a combined model, litter size also has a stronger esti- Statistical approaches mated effect on the distribution of plural breeding than body mass To test whether singular and plural breeders differ in their life- when both factors were standardized by subtracting each species’ history parameters, we ran binomial regression models using value from the mean across species divided by the standard devi- MCMCglmm (Hadfield and Nakagawa 2010) in the statistical soft- ation (effect of larger litter size on occurrence of plural breeding: ware R (R Core Team 2019). We first investigated whether differ - −11.4, 95% CI: −16.0 to −7.6, effect of larger body size: 3.3, 95% ences in monotocy/polytocy are associated with the distribution of CI: 1.4 to 5.4; 793 singular vs. 457 plural breeders). plural breeding. We included the phylogenetic relationship between Phylogenetic reconstructions provide further evidence of an as- species as covariance matrix, set a flat prior (Hadfield 2010) and sociation between the evolution of plural breeding and monotocy. used 1 500 000 iterations, a burn-in of 500 000 and a thinning in- Our phylogenetic reconstructions support previous evidence that terval of 10. Each analysis was repeated three times and visually the ancestor of mammals was polytocous and singular breeding inspected for convergence. We report the 95% confidence intervals (Lukas and Clutton-Brock 2013; Werneburg et  al. 2016). They (CIs) based on the Bayesian sample for all relationships to deter- show that the prevalence of monotocy or polytocy is comparatively mine whether an estimated effect is systematically different from stable within phylogenetic groups, with few evolutionary transitions 0.  The proportion of the Bayesian sample that crosses 0 is similar between monotocy and polytocy necessary to explain the distribu- to a P-value estimate; in all our cases, the CI did not contain 0 sug- tion of monotocy among the species in our sample (phylogenetic gesting that the results are robust. signal: K = 0.74; lambda 0.98; both P < 0.001). In contrast, plural For the phylogenetic reconstruction, we first estimated the breeding is more labile and, in several phyla, appears to have ori- strength of the phylogenetic signal for polytocy/monotocy and ginated relatively recently (phylogenetic signal: K  =  0.45; lambda singular/plural breeding using the function phylosig in PhyTools 0.95; both P < 0.001). (Revell 2012) in R to calculate the K-statistic and lambda, as- The evolution of plural breeding has occurred between 10 and sessing their significance by comparison to 10  000 simulations. 20 times more frequently in monotocous than in polytocous lin- To assess whether monotocy and plural breeding coevolved, eages (see Supplementary Material) and models assuming that we performed reconstructions using the function Discrete in monotocy and plural breeding evolved independently received BayesTraits V3 (Pagel et al. 2004). We ran models assuming either consistently less support than those indicating that the two traits an independent or a dependent evolution, estimating the param- are associated (median of log-likelihoods of independent models: eters using maximum likelihoods based on 100 tries per model −1105; median of log-likelihood of dependent models: −829). All specification. models that we explored suggest that evolutionary transitions from Downloaded from https://academic.oup.com/beheco/article/31/4/943/5830852 by DeepDyve user on 12 July 2022 Behavioral Ecology Monotocous Polytocous Plural breeder Singular breeder Plural breeder Singular breeder SIRENIA PROBOSCIDEA CETACEA PERISSODACTYLA TUBULIDENTATA PILOSA PHOLIDOTA HYRACOIDEA CHIROPTERA ARTIODACTYLA PRIMATES DIPROTODONTIA MACROSCELIDEA CINGULATA CARNIVORA AFROSORICIDA RODENTIA LAGOMORPHA SORICOMORPHA SCANDENTIA PERAMELEMORPHIA ERINACEOMORPHA DIDELPHIMORPHIA DASYUROMORPHIA 0% 20% 40% 60% 80%100% Figure 1 Proportion of species in mammalian Orders that records show to be either monotocous (in blue) or polytocous (in yellow) and either plural (dark shading) or singular breeders (plain colour). In Orders in which the majority of species are monotocous, such as cetaceans or primates, plural breeding is more likely than in Orders in which most species are polytocous, such as carnivores or rodents. polytocy to monotocy occur before transitions from singular to ancestral state to be monotocous and has a much lower likelihood plural breeding and that transitions to monotocy increase the prob- than the model assuming that transitions to plural breeding are ability of subsequent transitions from singular to plural breeding. more likely to occur in monotocous species. The most likely dependent model suggests that monotocy evolved in singular breeders and was only lost in relatively few instances DISCUSSION in plural breeders. Restricting the phylogenetic reconstructions to Our analysis supports the suggestion that interspecific contrasts in assume that the evolution of plural breeding was equally likely in sociality among breeding females are associated with variation in monotocous and polytocous lineages did not change the inference litter size and with the evolution of monotocy. Although 65% of that all monotocous plural breeders originated from monotocous all mammals are polytocous and polytocy is likely to have been the singular breeders: the model suggested that there have been no original ancestral condition for all live-bearing mammals (Myhrvold transitions to monotocy in plural breeders, with the only change et  al. 2015; Werneburg et  al. 2016), more than 85% of species in the model inference being a 10-fold increase in the rate at which where breeding units usually include more than one female that plural breeding would be lost in polytocous species. A model which breeds regularly are monotocous. Plural breeders produce smaller restricts both gains and losses of plural breeding to occur with litters than singular breeders and transitions from singular breeding equal probability in polytocous and monotocus species infers the Downloaded from https://academic.oup.com/beheco/article/31/4/943/5830852 by DeepDyve user on 12 July 2022 Lukas and Clutton-Brock • Monotocy and female sociality in mammals to plural breeding appear to have been substantially more frequent birds and insects, where females usually produce multiple eggs (de in monotocous lineages than in polytocous ones. Although plural Maghalaes and Costa 2009), cooperative and eusocial breeding ap- breeding and monotocy are both associated with diurnal activity, pears more common than plural breeding (Riehl 2013; Koenig and this association does not account for the association between plural Dickinson 2016; Rubenstein and Abbot 2017). breeding and monotocy, which persists when the effects of differ - The effects of phylogenetic contrasts in life-history patterns ences in activity timing are controlled. emphasize the need for comparative studies to focus at the most A likely reason for the association between plural breeding and appropriate taxonomic level. Where related species differ in their monotocy is that energy requirements of breeding females (espe- life-history parameters, analyses of the distributions of traits cially during lactation) are substantially higher in polytocous spe- within Orders can offer important insights into relationships be- cies, generating more intense competition between females for the tween contrasts in social behavior and variation in ecology and resources necessary to provision and raise offspring (Johnson et  al. life-history parameters (Rubenstein 1989; Kappeler and Pereira 2001; Speakman 2008). Although female interference in breeding 2003). However, where all members of the same Order share sim- attempts by other females is not confined to polytocous species, it ilar life-history characteristics, comparisons may need to span dif- appears to be more common in polytocous than monotocous spe- ferent radiations in order to identify the extent to which life-history cies: for example, physiological suppression of fertility in subor- parameters facilitate or constrain the evolution of social behavior dinate and female infanticide have been recorded to occur more (Harvey and Pagel 1991; Rubenstein and Abbott 2017). For ex- commonly in polytocous species than in monotocous ones (Clutton- ample, although there have been multiple analyses of the distri- Brock 2016; Lukas and Huchard 2019). bution of sociality in higher primates (Clutton-Brock and Harvey The association between monotocy and plural breeding may also 1980; Wrangham 1980; Sterck et al. 1997; Shultz et al. 2011), the help to explain contrasts in social behavior between major taxa— importance of monotocy on the evolution of sociality has (appar- and the nature of social relationships in particular. Comparative ently) not been previously recognized because a high proportion of studies show that rates of competitive interactions among group species are both monotocous and plural breeding. members tend to be reduced in mammals where average levels Finally, our analysis shows how differences in ecology, life of kinship between group members are relatively high and more history, and phylogeny are likely to interact in their effects on common when average kinship is low. In addition, costly forms of breeding systems and social organization. Although it is some- asymmetrical or altruistic cooperation, such as provisioning young times suggested that phylogenetic relationships, rather than con- born to others, are largely confined to species with high levels of trasts in ecology, control contrasts in social behavior between kinship and rare where average kinship between group members is higher level taxa (Gittleman 1986; Shultz and Dunbar 2007), low (Lukas and Clutton-Brock 2018). contrasts in life-history parameters between major taxonomic The association between plural breeding and monotocy raises groups are likely to represent ecological adaptations and to be questions about the evolution of monotocy itself. Within mammals, maintained by selection (Williams 1966; Lack 1968; Stearns the evolution of monotocy often appears to be associated with the 2000). Relationships between ecological variation and contrasts need for precociality in infants—either because they need to cling in social organization and reproductive strategies may conse- to their mothers or to the substrate (as in primates and bats) be- quently be less direct and may vary more widely between taxa cause they need to be able to locomote independently within a few than was recognized in early comparative studies. However, this hours of birth (as in many ungulates and cetaceans) or because variation does not contradict the view that contrasts in ecology young are exposed to potentially high levels of predation and there play a central role in guiding the evolution of interspecific differ - is a need to minimize the duration of the period of early develop- ences in social behavior and breeding systems. ment (as in the pinnipeds) (Martin and MacLarnon 1985; Kappeler 1998; Hamilton et  al. 2011). However, it is likely that the ecolog- SUPPLEMENTARY MATERIAL ical circumstances favoring monotocy differ between major animal groups (Promislow and Harvey 1990; Charnov 1991; Tökölyi et al. Supplementary data are available at Behavioral Ecology online. 2014) and this is too large a topic to consider in detail here. Our analysis illustrates the way in which contrasts in life-history FUNDING parameters can influence the evolution of sociality and the form of social behavior. Monotocy and the production of precocial This work was supported by the European Research Council (grant young may allow members of some species to occupy niches or 294494THCB2011). habitats where altricial young could not be reared but may, at the Conflict of interest: The authors have no financial or other conflicts of in- same time, preclude the evolution of some breeding systems. For terest to declare. example, among mammals, cooperative breeding systems, where group members other than their parents are principally respon- Data accessibility: Analyses reported in this article can be reproduced using sible for guarding and feeding infants, are restricted to polytocous the data provided by Lukas (2020). species, where average kinship between group members is rela- Handling editor: Michael Taborsky tively high (Lukas and Clutton-Brock 2012). This may be because, in monotocous species, helpers cannot generate large effects on the reproductive output of breeders or because monotocy reduces REFERENCES average kinship between group members to low levels, in partic- Agnani  P, Kauffmann  C, Hayes  LD, Schradin  C. 2018. Intra-specific ular in large groups, precluding the evolution of breeding systems variation in social organization of Strepsirrhines. Am J Primatol. involving costly forms of cooperation. 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Monotocy and the evolution of plural breeding in mammals

Lukas, Dieter; Clutton-Brock, Tim
Behavioral Ecology , Volume 31 (4) – Jul 29, 2020
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Downloaded from https://academic.oup.com/beheco/article/31/4/943/5830852 by DeepDyve user on 12 July 2022 applyparastyle "fig//caption/p[1]" parastyle "FigCapt" The official journal of the Behavioral ISBE Ecology International Society for Behavioral Ecology Behavioral Ecology (2020), 31(4), 943–949. doi:10.1093/beheco/araa039 Original Article Monotocy and the evolution of plural breeding in mammals a,b, a Dieter Lukas and Tim Clutton-Brock Department of Zoology, University of Cambridge, Downing Street, CB2 3EJ Cambridge, UK and Department of Human Behavior, Ecology and Culture, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103 Leipzig, Germany Received 7 August 2019; revised 6 March 2020; editorial decision 3 April 2020; accepted 14 April 2020. In many mammals, breeding females are intolerant of each other and seldom associate closely but, in some, they aggregate in groups that vary in size, stability, and kinship structure. Aggregation frequently increases competition for food, and interspecific differences in female sociality among mammals are commonly attributed to contrasts in ecological parameters, including variation in activity timing, the distribution of resources, as well as the risk of predation. However, there is increasing indication that differences in female soci- ality are also associated with phylogenetic relationships and with contrasts in life-history parameters. We show here that evolutionary transitions from systems where breeding females usually occupy separate ranges (“singular breeding”) to systems where breeding females usually aggregate (“plural breeding”) have occurred more frequently in monotocous lineages where females produce single young than in polytocous ones where they produce litters. A likely explanation of this association is that competition between breeding females for resources is reduced where they produce single young and is more intense where they produce litters. Our findings rein- force evidence that variation in life-history parameters plays an important role in shaping the evolution of social behavior. Key words: life history, social competition, sociality, phylogenetic reconstruction. INTRODUCTION these systems predominate within some Orders, including ungu- lates, cetaceans, and primates (Clutton-Brock 2016; Ward and In many mammals, adult females compete for access to resources Webster 2016). In most “plural breeders,” groups usually consist necessary to raise young and occupy separate ranges or territo- of breeding females born in the same group, as well as a number ries during the breeding season—as in many rodents, insectivores, of nonbreeding natal males that will eventually disperse to breed and nocturnal carnivores (Eisenberg 1983; Wolff and Sherman elsewhere, together with one or more immigrant males that fa- 2007; Clutton-Brock 2016). The ranges of breeding females in ther most of the young born in the group. In a small number of these “singular breeders” overlap to varying extents with those of species, groups consist of immigrant breeding females together neighboring females, as well as with those of males: in some, fe- with one or more natal breeding males (Clutton-Brock 1989; males defend exclusive territories against members of both sexes, Lukas and Clutton-Brock 2011). Intraspecific variation in group whereas, in others, they share their territories with particular males size is common (Richard 1974; Lott 1991) and, in some cases, but exclude other mature females; in some, there is extensive range groups in some populations usually contain multiple breeding fe- overlap between neighboring females, whereas, in others, breeding males, whereas, in others, many contain a single breeding female females share their ranges with nonbreeding relatives and unrelated (Schradin 2013). In many cases, this variation appears to reflect breeding males but forage separately; finally, in a few, breeding fe- contrasts in population density, with larger numbers of breeding males associate with nonbreeding relatives of both  sexes in cohe- females in groups where population densities are higher. sive groups as in the social mole-rats and some social mongooses Many comparative studies have explored the distribution of (Jarvis 1981; Clutton-Brock 2016). female group size in particular Orders of mammals and have In other species, breeding females are more tolerant of each shown that interspecific differences are related to variation in other and multiple breeding females share a common range and habitat use, feeding ecology, activity timing, and population den- form groups that include multiple individuals that breed regularly sity (Jarman 1974; Kaufmann 1974; Bradbury and Vehrencamp (Lewis and Pusey 1997; Clutton-Brock 2016). Although a rela- 1977; Clutton-Brock and Harvey 1977; Gittleman 1989; Wright tively small proportion of all mammals form groups of this kind, 1999; Fisher and Owens 2000; Ebensperger 2001), as well as to contrasts in body size, longevity, litter size, and juvenile develop- Address correspondence to D. Lukas. E-mail: [email protected] ment (Eisenberg 1983; van Schaik and Kappeler 1993; Rubenstein © The Author(s) 2020. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. Downloaded from https://academic.oup.com/beheco/article/31/4/943/5830852 by DeepDyve user on 12 July 2022 Behavioral Ecology and Abbot 2017; Smith et al. 2017). However, analyses of variation Here, we use comparative data for mammals and phylogenetic in female sociality seldom distinguish between groups that incor- reconstructions to investigate whether there is a consistent rela- porate several breeding females (plural breeders) and groups that tionship between the evolution of monotocy and the distribution include a single breeding female (singular breeders). The distinc- of plural breeding. Given that plural breeding is rarer and ap- tion between total group size and the number of breeding females parently the derived system, we investigated whether contem- that aggregate is important for it is the extent to which breeding porary mammals in which plural breeding has been observed at females aggregate that affects social and mating competition. When all are more likely to be monotocous, whereas species in which breeding females aggregate, the number of potential breeding part- only singular breeding occurs are more likely to be polytocous. ners that individual males can guard effectively is higher (Emlen To test the prediction that transitions to the production of single and Oring 1977), potentially increasing the intensity of sexual se- offspring remove constraints on aggregation in breeding females, lection on males (Kvarnemo and Ahnesjo 1996) and the extent we subsequently investigated whether any transitions to plural to which breeding males aggregate with each other (Andelman breeding have been more common in monotocous lineages than 1986). The number of breeding females in a group also affects so- in polytocous ones. cial interactions by influencing average levels of kinship between group members (Lukas et al. 2005; Lukas and Clutton-Brock 2018). Although contrasts in group size often reflect differences in the MATERIAL AND  METHODS number of breeding females that associate with each other, the re- Data and classifications lationship between total group size and the number of breeding females per group is inconsistent (Rubenstein et  al. 2016). For ex- We based the classification of the social system of mammals on our ample, some of the largest stable social groups found in mammals previous databases (Lukas and Clutton-Brock 2013, 2017a) and ex- occur in singular breeders, like naked mole-rats (Heterocephalus glaber) cluded the few mammalian species in which females produce eggs. where colonies can include several hundred individuals but only a We identified species as monotocous if median litter size was less single female breed in each group (Jarvis 1981; Braude 2000). than 1.5 and as polytocous if it was greater than 1.5. Data for litter Previous theories about the evolution of sociality among size (number of young per birth, central tendency across females in breeding females (plural breeding) have focused on its association wild populations), for adult body mass (female mass in grams, cen- with diurnal activity patterns and susceptibility to predation, as well tral tendency across females in both captive and wild populations), as with reliance on resources where direct competition between in- for diurnality (whether a species is strictly nocturnal or whether dividuals foraging in close proximity is not intense (Jarman 1974; part of its activity occurs during the day), and for diet (whether a Wrangham 1980). However, there are both theoretical and empir- species is a herbivore, carnivore, or omnivore) were obtained from ical reasons for expecting life-history parameters to also play an a combination of primary and secondary sources, including pub- important role. Lactating females experience substantial increases lished databases (Carey and Judge 2002; Ernest 2003; Bielby et al. in energetic requirements in all mammals and the energetic costs 2007; McCarthy et al. 2008; de Magalhaes and Costa 2009; Jones of raising young increase with litter size (Speakman 2008; Hamel et  al. 2009; Wilman et  al. 2014). If entries in these databases dif- et al. 2010; Hinde and Milligan 2011). As a result, competition be- fered slightly, we used the median value and, if entries were sub- tween coresident breeding females for resources necessary to raise stantially different, we referred to the primary literature to identify offspring is likely to be more intense in polytocous species (where the most likely value. females produce multiple young at once) than in monotocous ones We restricted species in our analysis to those for which field- (females produce single young). Comparative studies support this: based reports of social behavior were available (following Schradin for example, female infanticide appears to be more frequent in 2017; Lukas and Clutton-Brock 2017b). We identified species as polytocous than monotocous species (Lukas and Huchard 2019). In singular breeders if most females occupy separate home ranges addition, polytocy is usually associated with the production of rela- or territories during the breeding season (even if they share these tively altricial infants that need to be maintained in a nest or burrow with nonbreeding females or with males) and as plural breeders if (Eisenberg 1983; van Schaik and Kappeler 1993). As a result, many multiple breeding females share a common range and actively as- polytocous mammals are central place foragers (Stephens and sociate with each other (Ward and Webster 2016), forming groups Krebs 1986), which increases the energetic costs of aggregation in that usually include more than one individual that breeds regu- breeding females and so may constrain the evolution of sociality larly. Our definition of plural breeding includes fission–fusion spe- in breeding females (Kappeler 1998). Phylogenetic comparisons cies, such as chimpanzees where females may spend part of the also suggest that monotocy may facilitate the evolution of soci- day foraging independently but live in discrete communities that ality. Although singular breeding and polytocy appear to have been include multiple breeding females that share a common range. We the ancestral condition in many phylogenetic groups of mammals classified species that live in mixed sex pairs or in groups where (Leutenegger 1979; Lukas and Clutton-Brock 2013; Werneburg only a single female breeds regularly (like the social mole-rats, et  al. 2016), many of the mammalian taxa where plural breeding callitrichid primates, and several social mongooses) as singular is common are monotocous—including the primates, ungulates, breeders. We focus our classification of sociality on the behavior and cetaceans (Eisenberg 1983; Clutton-Brock 2016). Transitions to of breeding females, those that are in the later stages of preg- monotocy from polytocy appear to be rare and to have occurred at nancy or have dependent young and do not consider the beha- a relatively early stage in many mammalian lineages (Leutenegger vior of juveniles, males, or adult females who are not breeding. 1979; Bordes et  al. 2011; Werneburg et  al. 2016; Battistella et  al. In some species where breeding females commonly aggregate, 2019), whereas transitions in sociality appear to be more recent some breeding groups include a single breeding female, whereas (Blomberg et al. 2003; Kamilar and Cooper 2013), suggesting that others include several females that breed regularly (Nievergelt transitions to monotocy in these mammalian lineages might have et al. 2002; Dalerum 2007; Schradin et al. 2012; Weidt et al. 2014; removed constraints on the evolution of plural breeding. Valomy et al. 2015; Agnani et al. 2018; Miles et al. 2019). Where Downloaded from https://academic.oup.com/beheco/article/31/4/943/5830852 by DeepDyve user on 12 July 2022 Lukas and Clutton-Brock • Monotocy and female sociality in mammals intrapopulation variation of this kind was reported, we classified RESULTS species as plural breeders if, throughout the breeding season, most In the 1267 species in our sample, 44% were classified as breeding females are found in groups where several females breed monotocous and 56% as polytocous. In 54% of the mamma- regularly and as singular breeders if the majority of breeding fe- lian Orders represented in our sample, all species were either males were found in groups that included a single breeding female. monotocous or polytocous, whereas 46% of Orders included We used a majority rule to reduce risks of misclassification of rare both monotocous and polytocous species. Polytocy is predominant observations that are likely to be nonadaptive (following Schradin (more than 75%) in 10 of the 24 mammalian Orders represented et  al. 2018). In the small number of species where studies of dif- in our sample, whereas monotocy predominates in another 10 (see ferent populations have shown that plural breeding predominates Figure 1). in some populations or at some times, whereas singular breeding Although 56% of contemporary mammals in our sample predominates in others, often in association with relatively low are polytocous, more than 85% of all species classified as plural population density (e.g., striped mice; Schradin et  al. 2012), we breeders in our sample are monotocous and, in all seven Orders of classify them as plural breeders if plural breeding predominates mammals where plural breeding is common (artiodactyls, cetaceans, in either population as this is the rarer and derived system. It bats, diprotodons, perissodactyls, proboscidea, and primates), most has been suggested that, where multiple records of female group or all species are monotocous (see Figure  1). Compared with spe- size are available, they should be included as separate points (e.g. cies that we classified as singular breeders (and controlling for Miles et  al. 2019). However, like most other comparative studies, phylogenetic effects), plural breeding mammals have significantly we preferred to include a single value for each species in order smaller litter sizes (mean effect of larger litter size: −118.0, 95% to avoid particular species weighting our analyses disproportion- CI: −168.7 to −76.5; 810 singular vs. 457 plural breeders): among ately. We also generally do not have matching data on litter size singular breeders, median litter size is 3 and more than 80% of spe- for each population, so we cannot attempt to explain the full var- cies produce two or more offspring per breeding attempt. In con- iation in sociality across populations; we do not know the history trast, among species classified as plural breeders, median litter size of the populations within a given species, so we cannot infer if and is one and only 14% of species produce two or more offspring per how often transitions in sociality might have occurred (Stone et al. breeding attempt. 2011). The number of species for which multiple records showing The influence of litter size on the distribution of plural breeding differences in female sociality are available is relatively low and is independent of whether a species is nocturnal or diurnal (effect whether they are classified as plural or singular breeding does not of larger litter size on occurrence of plural breeding: −25.4, 95% appear to affect the outcome of our analyses. CI: −33.1 to −16.5; effect of being nocturnal rather than diurnal: For our phylogenetic reconstructions, we relied on a mamma- −8.9, 95% CI: −13.2 to −4.7; 374 singular vs. 115 plural breeders) lian supertree (Rolland et al. 2014) and did not resolve polytomies and whether it is omnivorous, herbivorous, or carnivorous (effect or modify the branch lengths in any analyses. All data and sources of larger litter size on occurrence of plural breeding: −19.7, 95% are deposited at the Knowledge Network for Biocomplexity (doi: CI: −27.8 to −11.4; effect of being herbivore rather than carnivore 10.5063/F1P8497S). or omnivore: 7.7, 95% CI: 0.5 to 15.7; 409 singular vs. 333 plural breeders). In a combined model, litter size also has a stronger esti- Statistical approaches mated effect on the distribution of plural breeding than body mass To test whether singular and plural breeders differ in their life- when both factors were standardized by subtracting each species’ history parameters, we ran binomial regression models using value from the mean across species divided by the standard devi- MCMCglmm (Hadfield and Nakagawa 2010) in the statistical soft- ation (effect of larger litter size on occurrence of plural breeding: ware R (R Core Team 2019). We first investigated whether differ - −11.4, 95% CI: −16.0 to −7.6, effect of larger body size: 3.3, 95% ences in monotocy/polytocy are associated with the distribution of CI: 1.4 to 5.4; 793 singular vs. 457 plural breeders). plural breeding. We included the phylogenetic relationship between Phylogenetic reconstructions provide further evidence of an as- species as covariance matrix, set a flat prior (Hadfield 2010) and sociation between the evolution of plural breeding and monotocy. used 1 500 000 iterations, a burn-in of 500 000 and a thinning in- Our phylogenetic reconstructions support previous evidence that terval of 10. Each analysis was repeated three times and visually the ancestor of mammals was polytocous and singular breeding inspected for convergence. We report the 95% confidence intervals (Lukas and Clutton-Brock 2013; Werneburg et  al. 2016). They (CIs) based on the Bayesian sample for all relationships to deter- show that the prevalence of monotocy or polytocy is comparatively mine whether an estimated effect is systematically different from stable within phylogenetic groups, with few evolutionary transitions 0.  The proportion of the Bayesian sample that crosses 0 is similar between monotocy and polytocy necessary to explain the distribu- to a P-value estimate; in all our cases, the CI did not contain 0 sug- tion of monotocy among the species in our sample (phylogenetic gesting that the results are robust. signal: K = 0.74; lambda 0.98; both P < 0.001). In contrast, plural For the phylogenetic reconstruction, we first estimated the breeding is more labile and, in several phyla, appears to have ori- strength of the phylogenetic signal for polytocy/monotocy and ginated relatively recently (phylogenetic signal: K  =  0.45; lambda singular/plural breeding using the function phylosig in PhyTools 0.95; both P < 0.001). (Revell 2012) in R to calculate the K-statistic and lambda, as- The evolution of plural breeding has occurred between 10 and sessing their significance by comparison to 10  000 simulations. 20 times more frequently in monotocous than in polytocous lin- To assess whether monotocy and plural breeding coevolved, eages (see Supplementary Material) and models assuming that we performed reconstructions using the function Discrete in monotocy and plural breeding evolved independently received BayesTraits V3 (Pagel et al. 2004). We ran models assuming either consistently less support than those indicating that the two traits an independent or a dependent evolution, estimating the param- are associated (median of log-likelihoods of independent models: eters using maximum likelihoods based on 100 tries per model −1105; median of log-likelihood of dependent models: −829). All specification. models that we explored suggest that evolutionary transitions from Downloaded from https://academic.oup.com/beheco/article/31/4/943/5830852 by DeepDyve user on 12 July 2022 Behavioral Ecology Monotocous Polytocous Plural breeder Singular breeder Plural breeder Singular breeder SIRENIA PROBOSCIDEA CETACEA PERISSODACTYLA TUBULIDENTATA PILOSA PHOLIDOTA HYRACOIDEA CHIROPTERA ARTIODACTYLA PRIMATES DIPROTODONTIA MACROSCELIDEA CINGULATA CARNIVORA AFROSORICIDA RODENTIA LAGOMORPHA SORICOMORPHA SCANDENTIA PERAMELEMORPHIA ERINACEOMORPHA DIDELPHIMORPHIA DASYUROMORPHIA 0% 20% 40% 60% 80%100% Figure 1 Proportion of species in mammalian Orders that records show to be either monotocous (in blue) or polytocous (in yellow) and either plural (dark shading) or singular breeders (plain colour). In Orders in which the majority of species are monotocous, such as cetaceans or primates, plural breeding is more likely than in Orders in which most species are polytocous, such as carnivores or rodents. polytocy to monotocy occur before transitions from singular to ancestral state to be monotocous and has a much lower likelihood plural breeding and that transitions to monotocy increase the prob- than the model assuming that transitions to plural breeding are ability of subsequent transitions from singular to plural breeding. more likely to occur in monotocous species. The most likely dependent model suggests that monotocy evolved in singular breeders and was only lost in relatively few instances DISCUSSION in plural breeders. Restricting the phylogenetic reconstructions to Our analysis supports the suggestion that interspecific contrasts in assume that the evolution of plural breeding was equally likely in sociality among breeding females are associated with variation in monotocous and polytocous lineages did not change the inference litter size and with the evolution of monotocy. Although 65% of that all monotocous plural breeders originated from monotocous all mammals are polytocous and polytocy is likely to have been the singular breeders: the model suggested that there have been no original ancestral condition for all live-bearing mammals (Myhrvold transitions to monotocy in plural breeders, with the only change et  al. 2015; Werneburg et  al. 2016), more than 85% of species in the model inference being a 10-fold increase in the rate at which where breeding units usually include more than one female that plural breeding would be lost in polytocous species. A model which breeds regularly are monotocous. Plural breeders produce smaller restricts both gains and losses of plural breeding to occur with litters than singular breeders and transitions from singular breeding equal probability in polytocous and monotocus species infers the Downloaded from https://academic.oup.com/beheco/article/31/4/943/5830852 by DeepDyve user on 12 July 2022 Lukas and Clutton-Brock • Monotocy and female sociality in mammals to plural breeding appear to have been substantially more frequent birds and insects, where females usually produce multiple eggs (de in monotocous lineages than in polytocous ones. Although plural Maghalaes and Costa 2009), cooperative and eusocial breeding ap- breeding and monotocy are both associated with diurnal activity, pears more common than plural breeding (Riehl 2013; Koenig and this association does not account for the association between plural Dickinson 2016; Rubenstein and Abbot 2017). breeding and monotocy, which persists when the effects of differ - The effects of phylogenetic contrasts in life-history patterns ences in activity timing are controlled. emphasize the need for comparative studies to focus at the most A likely reason for the association between plural breeding and appropriate taxonomic level. Where related species differ in their monotocy is that energy requirements of breeding females (espe- life-history parameters, analyses of the distributions of traits cially during lactation) are substantially higher in polytocous spe- within Orders can offer important insights into relationships be- cies, generating more intense competition between females for the tween contrasts in social behavior and variation in ecology and resources necessary to provision and raise offspring (Johnson et  al. life-history parameters (Rubenstein 1989; Kappeler and Pereira 2001; Speakman 2008). Although female interference in breeding 2003). However, where all members of the same Order share sim- attempts by other females is not confined to polytocous species, it ilar life-history characteristics, comparisons may need to span dif- appears to be more common in polytocous than monotocous spe- ferent radiations in order to identify the extent to which life-history cies: for example, physiological suppression of fertility in subor- parameters facilitate or constrain the evolution of social behavior dinate and female infanticide have been recorded to occur more (Harvey and Pagel 1991; Rubenstein and Abbott 2017). For ex- commonly in polytocous species than in monotocous ones (Clutton- ample, although there have been multiple analyses of the distri- Brock 2016; Lukas and Huchard 2019). bution of sociality in higher primates (Clutton-Brock and Harvey The association between monotocy and plural breeding may also 1980; Wrangham 1980; Sterck et al. 1997; Shultz et al. 2011), the help to explain contrasts in social behavior between major taxa— importance of monotocy on the evolution of sociality has (appar- and the nature of social relationships in particular. Comparative ently) not been previously recognized because a high proportion of studies show that rates of competitive interactions among group species are both monotocous and plural breeding. members tend to be reduced in mammals where average levels Finally, our analysis shows how differences in ecology, life of kinship between group members are relatively high and more history, and phylogeny are likely to interact in their effects on common when average kinship is low. In addition, costly forms of breeding systems and social organization. Although it is some- asymmetrical or altruistic cooperation, such as provisioning young times suggested that phylogenetic relationships, rather than con- born to others, are largely confined to species with high levels of trasts in ecology, control contrasts in social behavior between kinship and rare where average kinship between group members is higher level taxa (Gittleman 1986; Shultz and Dunbar 2007), low (Lukas and Clutton-Brock 2018). contrasts in life-history parameters between major taxonomic The association between plural breeding and monotocy raises groups are likely to represent ecological adaptations and to be questions about the evolution of monotocy itself. Within mammals, maintained by selection (Williams 1966; Lack 1968; Stearns the evolution of monotocy often appears to be associated with the 2000). Relationships between ecological variation and contrasts need for precociality in infants—either because they need to cling in social organization and reproductive strategies may conse- to their mothers or to the substrate (as in primates and bats) be- quently be less direct and may vary more widely between taxa cause they need to be able to locomote independently within a few than was recognized in early comparative studies. However, this hours of birth (as in many ungulates and cetaceans) or because variation does not contradict the view that contrasts in ecology young are exposed to potentially high levels of predation and there play a central role in guiding the evolution of interspecific differ - is a need to minimize the duration of the period of early develop- ences in social behavior and breeding systems. ment (as in the pinnipeds) (Martin and MacLarnon 1985; Kappeler 1998; Hamilton et  al. 2011). However, it is likely that the ecolog- SUPPLEMENTARY MATERIAL ical circumstances favoring monotocy differ between major animal groups (Promislow and Harvey 1990; Charnov 1991; Tökölyi et al. Supplementary data are available at Behavioral Ecology online. 2014) and this is too large a topic to consider in detail here. Our analysis illustrates the way in which contrasts in life-history FUNDING parameters can influence the evolution of sociality and the form of social behavior. Monotocy and the production of precocial This work was supported by the European Research Council (grant young may allow members of some species to occupy niches or 294494THCB2011). habitats where altricial young could not be reared but may, at the Conflict of interest: The authors have no financial or other conflicts of in- same time, preclude the evolution of some breeding systems. For terest to declare. example, among mammals, cooperative breeding systems, where group members other than their parents are principally respon- Data accessibility: Analyses reported in this article can be reproduced using sible for guarding and feeding infants, are restricted to polytocous the data provided by Lukas (2020). species, where average kinship between group members is rela- Handling editor: Michael Taborsky tively high (Lukas and Clutton-Brock 2012). This may be because, in monotocous species, helpers cannot generate large effects on the reproductive output of breeders or because monotocy reduces REFERENCES average kinship between group members to low levels, in partic- Agnani  P, Kauffmann  C, Hayes  LD, Schradin  C. 2018. Intra-specific ular in large groups, precluding the evolution of breeding systems variation in social organization of Strepsirrhines. Am J Primatol. involving costly forms of cooperation. 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