The influence of predator regime on the behaviour and mortality of a freshwater amphipod, Gammarus pulex
2011 Hydrobiologia, Co-authored with Kajsa Åbjörnsson and Christer Brönamrk
Download (.pdf) Soulsbury, C.D., Alatalo, R.V., Lebigre, C. & Siitari, H. (2012) Restrictive mate choice criteria causes age-specific inbreeding in female black grouse Tetrao tetrix. Animal Behaviour.
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Inbreeding is generally rare in large, natural populations yet mate choice often appears to be random with respect to... more Inbreeding is generally rare in large, natural populations yet mate choice often appears to be random with respect to kinship. This suggests that the risks of inbreeding may be small because passive mechanisms of inbreeding avoidance, for example dispersal, are effective at lowering inbreeding risk. Previous theoretical and empirical studies have assumed that the risks of inbreeding are constant over an individual's life span, but in the lek-breeding black grouse, inbreeding increases with female age. To determine whether inbreeding avoidance mechanisms are also age dependent, we generated four null models of random mate choice ranging from complete randomness to more biologically realistic mate choice criteria and compared these to 8 years of data on inbreeding levels at four different female age classes. We additionally tested whether mate fidelity decreased inbreeding risk. Observed inbreeding in female age classes 1, 2 or ≥3 were not significantly different from random, but was approximately 3.5 times higher in female age class ≥4. Alternative models using mate choice criteria showed no significant differences between observed and expected levels for any age class. Our results are in line with previous studies on noncooperatively breeding passerine birds, which indicate that mating is random with respect to kinship and that increased inbreeding in older females can be explained by reduced male availability caused by restrictive mate choice criteria. We also found that individuals that switched mates significantly increased relatedness to partners suggesting that mate fidelity may have evolved as an important passive inbreeding avoidance mechanism.
Antennal cropping during colony foundation in termites
ZooKeys 148: 185–196 (2011)
The literature on pairing and mating behavior in termites indicates that a number of distal antennal segments in... more The literature on pairing and mating behavior in termites indicates that a number of distal antennal segments in dealates of both sexes are often removed during colony foundation, with terms such as amputation, mutilation and cannibalism typically employed to report the phenomenon. Here we propose the use of the phrase ‘antennal cropping’ to describe the behavior, and assess naturally occurring levels of its occurrence by comparing the number of antennal segments in museum specimens of alates and dealates in 16 species of Australian termites (four families), supplemented by analyzing published data on Coptotermes gestroi. Dealates had significantly fewer antennal segments than alates in 14 of the 16 termite species, with both exceptions belonging to the family Termitidae. Levels of antennal cropping were not significantly different between the sexes but did vary by family. Dealates in the Kalotermitidae removed the most segments (41.3%) and those in the Termitidae removed the fewest (8.9%). We discuss the biological significance of this phylogenetically widespread termite behavior, and suggest that controlled antennal cropping is not only a normal part of their behavioral repertoire but also a key influence that changes the conduct and physiology of the royal pair during the initial stages of colony foundation.
Polygynandry, extra‐group paternity and multiple‐paternity litters in European badger (Meles meles) social groups
Authors:
HANNAH L. DUGDALE
DAVID W. MACDONALD
LISA C. POPE
TERRY BURKE
Published in:
Molecular Ecology
The costs and benefits of natal philopatry are central to the formation and maintenance of social groups. Badger... more The costs and benefits of natal philopatry are central to the formation and maintenance of social groups. Badger groups, thought to form passively according to the resource dispersion hypothesis (RDH), are maintained through natal philopatry and delayed dispersal; however, there is minimal evidence for the functional benefits of such grouping. We assigned parentage to 630 badger cubs from a high-density population in Wytham Woods, Oxford, born between 1988 and 2005. Our methodological approach was different to previous studies; we used 22 microsatellite loci to assign parent pairs, which in combination with sibship inference provided a high parentage assignment rate. We assigned both parents to 331 cubs at ≥ 95% confidence, revealing a polygynandrous mating system with up to five mothers and five fathers within a social group. We estimated that only 27% of adult males and 31% of adult females bred each year, suggesting a cost to group living for both sexes. Any strong motivation or selection to disperse, however, may be reduced because just under half of the paternities were gained by extra-group males, mainly from neighbouring groups, with males displaying a mixture of paternity strategies. We provide the strongest evidence to date for multiple-paternity litters, and for the first time show that within-group and extra-group males can sire cubs in the same litter. We investigate the factors that may play a role in determining the degree of delayed dispersal and conclude that the ecological constraints hypothesis, benefits of philopatry hypothesis, and life history hypothesis may all play a part, as proposed by the broad constraints hypothesis.
Material and genetic benefits of female multiple mating and polyandry
The maintenance of female polyandry has traditionally been attributed to the material (direct) benefits derived from... more The maintenance of female polyandry has traditionally been attributed to the material (direct) benefits derived from male mating resources (e.g. nuptial gifts) accrued by multiple mating. However, genetic (indirect) benefits offer amore robust explanation since only polyandrous, not monandrous, females may gain both material benefits from multiple mating and genetic benefits from multiple sires. Discriminating between material and genetic benefits is essential when addressing the mechanism by which polyandry is adaptively maintained, but are difficult to disentangle because they affect fitness in similar ways. To test the hypothesis that genetic benefits maintain polyandry, we compared four components of fitness (longevity, fecundity, hatching success and survivorship) between monandrous and polyandrous females in the ground cricket, Allonemobius socius. We discovered that females derived nongenetic benefits from mating multiply, in that the magnitude of the nuptial gift was positively associated with the number of eggs produced. However, polyandrous females had over a two-fold greater hatching success and a 43% greater offspring survivorship, leading to a significantly higher relative fitness than the monandrous strategy. These results were independent of the confounding effects of material benefits, implying that genetic contributions play a large role in the maintenance of polyandry and potentially in the antagonistic coevolutionary relationship between polyandry and male nuptial gifts.
USO DELLO SPAZIO DURANTE IL PERIODO DEGLI ACCOPPIAMENTI IN FEMMINE DI CAPRIOLO
by Luca Börger
Hystrix - The Italian Journal of Mammalogy (2005). Conference proceedings co-authored with Fiora Meschi (first author), Novella Franconi, Francesco Ferretti, Giampiero De Michele and Sandro Lovari
Roe deer mating tactics
by Luca Börger
PhD thesis (2006; University of Cambridge, UK)
The thesis investigates the causes and consequences of individual differences in mating behaviour, using roe deer as a... more The thesis investigates the causes and consequences of individual differences in mating behaviour, using roe deer as a case study. A literature review identified two general themes, the interplay between natural and sexual selection and the importance of considering mutual mate choice and sexual conflict. These themes both suggest that variance in individual performance in mating success may be ultimately determined by ecological or behavioural processes. Given this, a crucial factor influencing individual differences in mating strategy is space use, as spatio-temporal variance of mating opportunities generates variance in selection pressures. To investigate space use, a total of 48 animals were radiotracked over four years in a study area in central Italy. Three currently unsolved methodological problems were addressed by developing new analytical approaches: identifying the most appropriate combination between sampling protocol and home range estimation method, estimating spatial variance in radiotracking error, and decomposing variance in home range size into components due to variation in temporal, spatial, and individual-level processes. The findings contrast with several common assumptions about roe deer space use and mating behaviour. Second, territoriality is the predominant male mating behaviour in roe deer. Understanding the decision-making mechanisms determining the location of territory boundaries is crucial for comprehending how animal territories form. The predictions of a recent model on the role of landmarks as a convention during territory delineation were tested by setting up a line of artificial landmarks between territories located in open areas. According to model predictions, the experimental treatment caused a shift in space use and scent marking behaviour, rate of agonistic interactions, and priority of access to females. However, in several cases the convention was not accepted, and the reasons are discussed. Third, roe deer mating behaviour and space use was observed over four rutting seasons on 75 individuals in total. The ecological and life-history determinants of variance in mating behaviour were identified, showing previously unknown status-dependent differences between adult males and females. Evidence for male competition and female choice, but also male choice and female competition, as well as the potential for sexual conflict, is presented. It is concluded that territoriality is a male mating strategy determined by male competition. The availability of females, in relation to ecological variables, determines the pay-offs of the alternative tactics, like stay inside the territory, sneak matings, or challenge and evict another territory owner. Females adopt a conditional space use strategy, where the tactics (stay and compete, mate outside the home range) depend on the availability of males and the competition from other females within the home range. The classical view of roe deer mating system as an example of classical resource defence polygyny is not supported.
Reproductive Social Behavior: Ignoring Ecological Scenarios and the "Currency" of Evolution
by Luca Börger
Science (2006); E-letter co-authored with F. Pelletier.
We disagree with the idea of Roughgarden et al. that because sexual reproduction is cooperative it can only be... more We disagree with the idea of Roughgarden et al. that because sexual reproduction is cooperative it can only be understood in a cooperative framework that ignores conflict. In our view, it is conflict that has generated the array of sex-specific traits that we observe in nature.
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Polyandry by wood mice in natural populations
by Warren Booth
Co-authored with: W. I. Montgomery & P. A. Prodohl
Multiple paternity was investigated for the first time in natural populations of the wood mouse Apodemus sylvaticus.... more Multiple paternity was investigated for the first time in natural populations of the wood mouse Apodemus sylvaticus. Thirteen females and their respective litters sampled within distinct habitats, seasons and years were screened for eight microsatellite loci. Allelic variation was compared with a dataset comprising 307 adult mice collected from the same source populations as pregnant females. Multiple paternity was unambiguously identified in seven litters (53.8%). In each case, a minimum of two or three male parents were involved. Populations of A. sylvaticus inhabiting the northern latitudes of the species range are characterized by annual cycles of abundance during which numbers can fluctuate by several orders of magnitude. Hence, the discovery of multiple paternity within litters sampled between May and July (high and low densities, respectively) in all years suggests that polyandry maximizes genetic diversity of the litter and, hence, survival of some of the offspring through such cycles. The results indicate that polyandry is a common mode of reproduction within wild populations of A. sylvaticus.
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Sexual conflict in primates
Sexual conflict is increasingly recognized as a major force for evolutionary change and holds great potential for... more Sexual conflict is increasingly recognized as a major force for evolutionary change and holds great potential for delineating variation in primate behavior and morphology. The goals of this review are to highlight the rapidly rising field of sexual conflict and the ongoing shift in our understanding of interactions between the sexes. We discuss the evidence for sexual conflict within the Order Primates, and assess how studies of primates have illuminated and can continue to increase our understanding of sexual conflict and sexual selection. Finally, we introduce a framework for understanding the behavioral, anatomical, and genetic expression of sexual conflict across primate mating systems and suggest directions for future research.
The evolution of social behaviour: the effect of mating system and social structure in the European badger Meles meles
Author:
Hannah L Dugdale
DPhil thesis. University of Oxford, Oxford. pp 282
Studies of mating systems and social organisation have been central to understanding of the evolution of social... more Studies of mating systems and social organisation have been central to understanding of the evolution of social behaviour. The European badger Meles meles is a good species in which to study these processes, as its complex social system provides an opportunity to investigate how both natural and kin selection shape the evolution of mating systems and social structure. In this thesis, I use behavioural and genetic data to describe the mating system and social organisation of a high-density badger population and examine the occurrence of cooperative breeding. I genotyped 915 (85%) badgers trapped in Wytham Woods (1987–2005), 630 of which were cubs, and assigned both parents to 331 cubs with 95% confidence. This revealed a polygynandrous mating system, with up to five mothers and five fathers per social group. Mounting behaviour was also polygynandrous and I show the strongest evidence to date for multiple-paternity litters. I demonstrate, for the first time, that groups consisted of close and distant kin: approximately one third of group members were first-order kin, and overall group members had slightly lower relatedness levels than half-siblings. Within groups, adult and yearling females had higher pairwise relatedness than males, and neighbouring groups contained relatives. These findings result from the high level (42%) of extra-group paternities, 86% of which were assigned to neighbouring males. For the first time I show that females avoided inbreeding by mating with extra-group males; however, incestuous matings did occur. Promiscuous and repeated mountings were observed, which may reduce male–male aggression and infanticide, but may also promote sperm competition, genetic diversity, and / or genetic compatibility. Just under a third of adult males and females were assigned parentage each year and I quantify, for the first time, reproductive skew within badger groups. Correlations between relatedness, group productivity, and reproductive skew were not consistent with the predictions of incomplete-control models; rather, resource availability may play a role. Older and younger badgers displayed reduced annual breeding success, with male success increasing initially with experience. The Restraint, Constraint, and Selection Hypotheses did not explain the age-related breeding pattern in females. Variance in lifetime breeding success (LBS) was greater for males. Males that only bred within or only outside of their groups had half the LBS of males that did both. Females that were assigned maternity probably bred cooperatively and allonursed non-offspring, which has not been demonstrated previously. No benefit was established, however, in terms of litter size, probability of offspring breeding, or offspring lifetime breeding success, with more mothers in a group. In conclusion, badger social groups are fostered through kinship ties. Polygynandry and repeated mounting may have evolved originally to reduce male–male aggression and infanticide by males, through paternity masking. Although plural breeding occurs, group living appears to be costly. Motivation to disperse may be reduced through high-levels of extra-group paternities, which may also reduce inbreeding. Cooperative breeding among mothers may represent a low-cost behaviour with indirect benefits due to high levels of relatedness between female group-members. Badger sociality therefore represents an early stage in the evolution of social behaviour.
Soulsbury, C.D., Alatalo, R.V., Lebigre, C., Rokka, K. & Siitari, H. (2011) Age-dependent inbreeding risk and offspring fitness costs in female black grouse. Biology Letters, 7: 853-855.
Dispersal is an important mechanism used to avoid inbreeding. However, dispersal may only be effective for part of an... more Dispersal is an important mechanism used to avoid inbreeding. However, dispersal may only be effective for part of an individual’s lifespan since, post-dispersal individuals that breed over multiple reproductive events may risk mating with kin of the philopatric sex as they age. We tested this hypothesis in black grouse Tetrao tetrix, and show that yearling females never mated with close relatives whereas older females did. However, matings were not with direct kin suggesting that short-distance dispersal to sites containing kin and subsequent overlap of reproductive lifespans between males and females was causing this pattern. Chick mass was lower when kinship was high, suggesting important fitness costs associated with inbred matings. This study shows that increased inbreeding risk might be a widespread yet rarely considered cost of ageing.
Soulsbury, C.D., Iossa, G., Baker, P.J., White, P.C.L. & Harris, S. (2011) Behavioral and spatial analysis of extraterritorial movements in red foxes (Vulpes vulpes). Journal of Mammalogy, 92, 190-199.
Movements away from the natal or home territory are important to many ecological processes, including gene flow,... more Movements away from the natal or home territory are important to many ecological processes, including gene flow, population regulation, and disease epidemiology, yet quantitative data on these behaviors are lacking. Red foxes exhibit 2 periods of extraterritorial movements: when an individual disperses and when males search neighboring territories for extrapair copulations during the breeding season. Using radiotracking data collected at 5-min interfix intervals, we compared movement parameters, including distance moved, speed of movement, and turning angles, of dispersal and reproductive movements to those made during normal territorial movements; the instantaneous separation distances of dispersing and extraterritorial movements to the movements of resident adults; and the frequency of locations of 95%, 60%, and 30% harmonic mean isopleths of adult fox home territories to randomly generated fox movements. Foxes making reproductive movements traveled farther than when undertaking other types of movement, and dispersal movements were straighter. Reproductive and dispersal movements were faster than territorial movements and also differed in intensity of search and thoroughness. Foxes making dispersal movements avoided direct contact with territorial adults and moved through peripheral areas of territories. The converse was true for reproductive movements. Although similar in some basic characteristics, dispersal and reproductive movements are fundamentally different both behaviorally and spatially and are likely to have different ultimate purposes and contrasting effects on spatial processes such as disease transmission.
Iossa, G., Soulsbury, C.D., Baker, P.J., Edwards, K.E. & Harris, S. (2009) Behavioral changes associated with a population density decline in the facultatively social red fox. Behavioral Ecology, 20: 385-395.
Understanding the causal mechanisms promoting group formation in carnivores has been widely investigated, particularly... more Understanding the causal mechanisms promoting group formation in carnivores has been widely investigated, particularly how fitness components affect group formation. Population density may affect the relative benefits of natal philopatry versus dispersal. Density effects on individual behavioral strategies have previously been studied through comparisons of different populations, where differences could be confounded by between-site effects. We used a single population of red foxes (Vulpes vulpes) in the city of Bristol, UK, that underwent a natural perturbation in density to compare key changes in 1) group structure, 2) within-group relatedness, 3) mating system, 4) dispersal, and 5) dominance attainment. At high densities (19.6–27.6 adults km−2), group sex ratios were equal and included related and unrelated individuals. At low densities (4.0–5.5 adults km−2), groups became female biased and were structured around philopatric females. However, levels of within-group relatedness were unchanged. The genetic mating patterns changed with no instances of multiple-paternity litters and a decline in the frequency of extrapair litters of cubs from ≤77% to ≤38%. However, the number of genetically monogynous groups did not differ between periods. Dispersal was male biased at both high and low densities. At high density, most dominant males in the study groups appeared to have gained dominance after dispersing, but natal philopatry was an equally successful strategy at low density; conversely, most dominant females were philopatric individuals at both high and low densities. These results illustrate how density may alter behavioral strategies such as mating patterns and how this, in turn, alters group structure in a single population.
Soulsbury, C.D. (2010) Ovulation mode modifies paternity monopolization in mammals. Biology Letters, 6: 39-41.
There are two forms of ovulation: spontaneous and induced. As copulation triggers ovulation for induced ovulators,... more There are two forms of ovulation: spontaneous and induced. As copulation triggers ovulation for induced ovulators, males can predict the timing of ovulation and may have greater paternity monopolization than spontaneous ovulators. However, this prediction has never, to my knowledge, been tested. Using a cross-species comparison I examined the percentage of offspring sired within a litter (single paternity) and in social species the percentage of offspring sired by the dominant male (alpha paternity). My results indicate that ovulation mode alters the ability of males to monopolize paternity, with males of induced ovulators having higher single paternity and greater alpha paternity where male–female association is intermittent.
Iossa, G., Soulsbury, C.D., Baker, P.J. & Harris, S. (2008) Sperm competition and the evolution of testes size in terrestrial mammalian carnivores. Functional Ecology, 22: 655-662.
1. Understanding the factors influencing variation in the degree of sperm competition is a key question underlying the... more
1. Understanding the factors influencing variation in the degree of sperm competition is a key question underlying the mechanisms driving sexual conflict.
2. Previous behavioural and comparative studies have indicated that carnivores appear to have evolved under sperm competition but an analysis of the predictors of the level of sperm competition is missing.
3. In this study, we use phylogenetic comparative methods to investigate life-history parameters predicted to affect the degree of sperm competition in terrestrial carnivores using variation in relative testes size (RTS, after controlling for body size allometry) as a measure of the level of sperm competition. Due to a paucity of consistent data across taxa, we used three measures of RTS: testes mass (n = 40 species), testes and epididymes mass combined (n = 38), and testes volume (n = 48). We also created a derived data set (n = 79) with testes mass estimated from regression analyses on the other measures of testes size.
4. Carnivores with shorter mating seasons had relatively larger testes, consistent with the hypothesis that sperm competition is greater when the degree of female oestrous synchrony is high. This relationship was stronger in spontaneous versus induced ovulators, suggesting higher sperm competition levels in spontaneous ovulators. This is the first comparative study to show this within mammalian taxa. Neither social mating system nor reproductive lifespan were significantly associated with variation in RTS and hence are poor predictors of sperm competition levels.
5. None of the above relationships were found to be significant for the testes and epididymes mass combined data set, but our understanding of the role of the epididymis in sperm competition is too limited to draw any conclusions.
6. Finally, we consistently found a significant phylogenetic signal in all analyses, indicating that phylogeny has played a significant role in the evolution of carnivore testes size and, therefore, in shaping levels of sperm competition.
7. Our results shed new light into the factors affecting levels of sperm competition in terrestrial carnivores by showing that the degree of oestrous synchrony and ovulation type interact to predict variation in RTS.
Iossa, G., Soulsbury, C.D., Baker, P. & Harris, S. (2008) Body mass, territory size, and life-history tactics in a socially monogamous canid, the red fox Vulpes vulpes. Journal of Mammalogy, 89: 1481-1490.
Male-biased sexual size dimorphism is typical of polygynous mammals, where the degree of dimorphism in body mass is... more Male-biased sexual size dimorphism is typical of polygynous mammals, where the degree of dimorphism in body mass is related to male intrasexual competition and the degree of polygyny. However, the importance of body mass in monogamous mammals is largely unknown. We investigated the effect of body mass on life-history parameters and territory size in the red fox (Vulpes vulpes), a socially monogamous canid with slight sexual dimorphism. Increased body size in males appeared to confer an advantage in territory acquisition and defense contests because heavier males held larger territories and exerted a greater boundary pressure on smaller neighbors. Heavier male foxes invested more effort in searching for extrapair matings by moving over a wider area and farther from their territories, leading to greater reproductive success. Males that sired cubs outside their own social group appeared to be heavier than males that only sired cubs within their social group or that were cuckolded, but our results should be treated with caution because sample sizes were small. Territory size, boundary pressure, and paternity success were not related to age of males. In comparison, body mass of females was not related to territory size, probability of breeding, litter size, or cub mass. Only age affected probability of breeding in females: younger females reproduced significantly less than did older females, although we did not measure individual nutritional status. Thus, body mass had a significant effect on life-history traits and territory size in a socially monogamous species comparable to that reported in polygynous males, even in the absence of large size dimorphism.