skip to main content


Title: Multilevel selection on social network traits differs between sexes in experimental populations of forked fungus beetles
Abstract

Both individual and group behavior can influence individual fitness, but multilevel selection is rarely quantified on social behaviors. Social networks provide a unique opportunity to study multilevel selection on social behaviors, as they describe complex social traits and patterns of interaction at both the individual and group levels. In this study, we used contextual analysis to measure the consequences of both individual network position and group network structure on individual fitness in experimental populations of forked fungus beetles (Bolitotherus cornutus) with two different resource distributions. We found that males with high individual connectivity (strength) and centrality (betweenness) had higher mating success. However, group network structure did not influence their mating success. Conversely, we found that individual network position had no effect on female reproductive success but that females in populations with many social interactions experienced lower reproductive success. The strength of individual-level selection in males and group-level selection in females intensified when resources were clumped together, showing that habitat structure influences multilevel selection. Individual and emergent group social behavior both influence variation in components of individual fitness, but impact the male mating success and female reproductive success differently, setting up intersexual conflicts over patterns of social interactions at multiple levels.

 
more » « less
NSF-PAR ID:
10402119
Author(s) / Creator(s):
; ; ;
Publisher / Repository:
Oxford University Press
Date Published:
Journal Name:
Evolution
Volume:
77
Issue:
1
ISSN:
0014-3820
Format(s):
Medium: X Size: p. 289-303
Size(s):
["p. 289-303"]
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Male mating strategies respond to female availability such that variation in resources that affect spatial distribution can also alter cost–benefit tradeoffs within a population. In arid‐adapted species, rainfall alters reproduction, behavior, morphology, and population density such that populations differing in resource availability may also differ in successful reproductive strategies. Here, we compare two populations of Cape ground squirrels (Xerus inauris), a sub‐Saharan species with year‐round breeding and intense mating competition. Unlike most mammals where males resort to aggressive interactions over females, maleX. inaurisare tolerant of one another, relying instead on other nonaggressive pre‐ and postcopulatory strategies to determine reproductive success. Our findings suggest that differences in resource availability affect female distribution, which ultimately leads to intraspecific variation in male reproductive tactics and sexual morphology. Sperm competition, assessed by reproductive morphometrics, was more pronounced in our high resource site where females were distributed evenly across the landscape, whereas dominance seemed to be an important determinant of success in our low resource site where females were more aggregated. Both sites had similar mating intensities, and most males did not sire any offspring. However, our low resource site had a higher variance in fertilization success with fewer males siring multiple offspring compared with our high resource site where more individuals were successful. Our results lend support to resource models where variations in female spatial distribution attributed to environmental resources ultimately impact male reproductive behaviors and morphology.

     
    more » « less
  2. Applegate, Roger (Ed.)
    Abstract - Odocoileus virginianus (White-tailed Deer) are social animals that thrive in rural and urban settings. Scraping behavior is an olfactory reproductive communication used by White-tailed Deer to establish breeding networks. Male scraping is a complex scent-marking behavior which advertises sociosexual status and location to potential females as well as to competing males. Female scraping behavior is thought to be an estrus signal alerting males during times of optimal fertility. This study describes a new method to examine White-tailed Deer mating systems using social network analyses of scraping behavior using an urban population of White-tailed Deer as a model. First, we validated the scraping behavior at our study site in Tougaloo, MS, during the 2019–2020 breeding season. Using remote monitoring, we continuously documented scraping behaviors over 8 different scrape-site locations and found similar behavioral, temporal, and spatial patterns in our urban breeding network as reported in rural and captive deer studies. Next, we describe methods detailing how social network analyses can reveal sociality, dominance, importance, and social structure within male scraping networks. Using centrality measures, we were able to rank dominant male influencers, anticipate social conflict among rivals, and made predictions regarding the spread of communicable diseases through a male scraping network. We also detail network analyses combining both male and female scraping behavior to reveal a glimpse into the complexity of breeding networks. Using network measures, we were able to rank males based on competitiveness and female preference. Lastly, we generated a theoretical breeding network to explore female sociability, competitiveness, preference, and mate choice. Taken together, this work describes a new method using scraping network analysis to investigate the complexity of White-tailed Deer breeding networks. This work also demonstrates the future applications of this method for predicting the spread of communicable diseases and for predicting mate selection within White-tailed Deer mating systems. 
    more » « less
  3. Abstract

    Selection that acts in a sex-specific manner causes the evolution of sexual dimorphism. Sex-specific phenotypic selection has been demonstrated in many taxa and can be in the same direction in the two sexes (differing only in magnitude), limited to one sex, or in opposing directions (antagonistic). Attempts to detect the signal of sex-specific selection from genomic data have confronted numerous difficulties. These challenges highlight the utility of “direct approaches,” in which fitness is predicted from individual genotype within each sex. Here, we directly measured selection on Single Nucleotide Polymorphisms (SNPs) in a natural population of the sexually dimorphic, dioecious plant, Silene latifolia. We measured flowering phenotypes, estimated fitness over one reproductive season, as well as survival to the next year, and genotyped all adults and a subset of their offspring for SNPs across the genome. We found that while phenotypic selection was congruent (fitness covaried similarly with flowering traits in both sexes), SNPs showed clear evidence for sex-specific selection. SNP-level selection was particularly strong in males and may involve an important gametic component (e.g., pollen competition). While the most significant SNPs under selection in males differed from those under selection in females, paternity selection showed a highly polygenic tradeoff with female survival. Alleles that increased male mating success tended to reduce female survival, indicating sexual antagonism at the genomic level. Perhaps most importantly, this experiment demonstrates that selection within natural populations can be strong enough to measure sex-specific fitness effects of individual loci.

    Males and females typically differ phenotypically, a phenomenon known as sexual dimorphism. These differences arise when selection on males differs from selection on females, either in magnitude or direction. Estimated relationships between traits and fitness indicate that sex-specific selection is widespread, occurring in both plants and animals, and explains why so many species exhibit sexual dimorphism. Finding the specific loci experiencing sex-specific selection is a challenging prospect but one worth undertaking given the extensive evolutionary consequences. Flowering plants with separate sexes are ideal organisms for such studies, given that the fitness of females can be estimated by counting the number of seeds they produce. Determination of fitness for males has been made easier as thousands of genetic markers can now be used to assign paternity to seeds. We undertook just such a study in S. latifolia, a short-lived, herbaceous plant. We identified loci under sex-specific selection in this species and found more loci affecting fitness in males than females. Importantly, loci with major effects on male fitness were distinct from the loci with major effects on females. We detected sexual antagonism only when considering the aggregate effect of many loci. Hence, even though males and females share the same genome, this does not necessarily impose a constraint on their independent evolution.

     
    more » « less
  4. Abstract The reproductive biology of many female mammals is affected by their social environment and their interactions with conspecifics. In mammalian societies structured by linear dominance hierarchies, such as that of the spotted hyena (Crocuta crocuta), a female’s social rank can have profound effects on both her reproductive success and her longevity. In this species, social rank determines priority of access to food, which is the resource limiting reproduction. Due largely to rank-related variation in access to food, reproduction from the perspective of a female spotted hyena can only be understood in the context of her position in the social hierarchy. In this review, we examine the effects of rank on the various phases of reproduction, from mating to weaning. Summed over many individual reproductive lifespans, the effect of rank at these different reproductive phases leads to dramatic rank-related variation in fitness among females and their lineages. Finally, we ask why females reproduce socially despite these apparent costs of group living to low-ranking females. Gregariousness enhances the fitness of females regardless of their positions in the social hierarchy, and females attempting to survive and reproduce without clanmates lose all their offspring. The positive effects of gregariousness appear to result from having female allies, both kin and non-kin, who cooperate to advertise and defend a shared territory, acquire, and defend food resources, maintain the status quo, and occasionally also to rise in social rank. 
    more » « less
  5. Abstract

    The primate adolescent period is characterized by a series of changes in physiology, behavior, and social relationships. Orangutans have the slowest life history and the longest period of dependency of all primates. As members of a semisolitary species with high levels of sexual coercion, adolescent female orangutans face a unique combination of challenges when achieving independence from their mother. This study examined the mating behavior of adolescent female orangutans and compared it with that of adult females to assess whether mating behavior reflects distinct strategies at these different points in the life cycle. Data were collected in Gunung Palung National Park on the island of Borneo over 20 years. Mating events from adolescent (n = 19) and adult females (n = 26) were scored and compared. Adolescent female mating events had significantly higher mating scores (indicating more proceptivity) than those of adult females (β = 1.948,p = .001). Adolescent females also engaged in elaborate sociosexual interactions with different flanged males, behaviors that were never observed during mating events of adult females. These interactions involved characteristic behavior on the part of both the adolescent females and the flanged males. Given these findings and the documentation of similar accounts of adolescent female–flanged male mating from the island of Sumatra, we propose that adolescent female orangutans display distinctive behavioral repertoires throughout the genusPongowhich serves to overcome male ambivalence toward nulliparous females, establish familiarity, and evaluate coercive tendencies in flanged males. We suggest that these behavioral patterns are an integral part of female social development in a female philopatric, but highly dispersed species where consistent social support is absent after ranging independence is achieved.

     
    more » « less