Reproductive asynchrony in natural butterfly populations and its consequences for female matelessness
TL;DR: These analyses provide the first direct, quantitative evidence of female reproductive failure due to asynchrony in small natural populations, and suggest that reproductive as synchrony exerts a strong and largely unappreciated influence on the population dynamics of these butterflies and other species with similarly asynchronous reproductive phenology.
Abstract: Summary 1. Reproductive asynchrony, where individuals in a population are short-lived relative to the population-level reproductive period, has been identified recently as a theoretical mechanism of the Allee effect that could operate in diverse plant and insect species. The degree to which this effect impinges on the growth potential of natural populations is not yet well understood. 2. Building on previous models of reproductive timing, we develop a general framework that allows a detailed, quantitative examination of the reproductive potential lost to asynchrony in small natural populations. 3. Our framework includes a range of biologically plausible submodels that allow details of mating biology of different species to be incorporated into the basic reproductive timing model. 4. We tailor the parameter estimation methods of the full model (basic model plus mating biology submodels) to take full advantage of data from detailed field studies of two species of Parnassius butterflies whose mating status may be assessed easily in the field. 5. We demonstrate that for both species, a substantial portion of the female population (6·5‐ 18·6%) is expected to die unmated. These analyses provide the first direct, quantitative evidence of female reproductive failure due to asynchrony in small natural populations, and suggest that reproductive asynchrony exerts a strong and largely unappreciated influence on the population dynamics of these butterflies and other species with similarly asynchronous reproductive phenology.
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TL;DR: It is shown that unifying two well-known lines of thinking provides the necessary conceptual framework to account for variation in sexual selection and how this can produce selection for mate acquisition traits despite naturally selected costs.
Abstract: What explains variation in the strength of sexual selection across species, populations or differences between the sexes? Here, we show that unifying two well-known lines of thinking provides the necessary conceptual framework to account for variation in sexual selection. The Bateman gradient and the operational sex ratio (OSR) are incomplete in complementary ways: the former describes the fitness gain per mating and the latter the potential difficulty of achieving it. We combine this insight with an analysis of the scope for sexually selected traits to spread despite naturally selected costs. We explain why the OSR sometimes does not affect the strength of sexual selection. An explanation of sexual selection becomes more logical when a long ‘dry time’ (‘time out’, recovery after mating due to e.g. parental care) is understood to reduce the expected time to the next mating when in the mating pool (i.e. available to mate again). This implies weaker selection to shorten the wait. An integrative view of sexual selection combines an understanding of the origin of OSR biases with how they are reflected in the Bateman gradient, and how this can produce selection for mate acquisition traits despite naturally selected costs.
159 citations
Cites background from "Reproductive asynchrony in natural ..."
...Although this is demonstrably false in some systems (Calabrese et al. 2008; Rhainds 2010), the conceptual issue raised is important regardless of whether any females remain unmated in a given species: given a potentially non-linear graph, where do we quantify the slope between reproductive and…...
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TL;DR: In this article, the authors identify traits that are predicted to co-vary with dispersal and investigate the correlations that may constrain dispersal using published information on butterflies, finding that dispersal directly correlated with demographic traits, mostly fecundity, whereas phylogenetic relationships among species had a negligible influence on this pattern, gene flow and individual movements are correlated with ecological specialisation and body size, respectively and routine movements only affected short-distance dispersal.
Abstract: As dispersal plays a key role in gene flow among populations, its evolutionary dynamics under environmental changes is particularly important. The inter-dependency of dispersal with other life history traits may constrain dispersal evolution, and lead to the indirect selection of other traits as a by-product of this inter-dependency. Identifying the dispersalOs relationships to other life-history traits will help to better understand the evolutionary dynamics of dispersal, and the consequences for species persistence and ecosystem functioning under global changes. Dispersal may be linked to other life-history traits as their respective evolutionary dynamics may be interdependent, or, because they are mechanistically related to each other. We identify traits that are predicted to co-vary with dispersal, and investigated the correlations that may constrain dispersal using published information on butterflies. Our quantitative analysis revealed that (1) dispersal directly correlated with demographic traits, mostly fecundity, whereas phylogenetic relationships among species had a negligible influence on this pattern, (2) gene flow and individual movements are correlated with ecological specialisation and body size, respectively and (3) routine movements only affected short-distance dispersal. Together, these results provide important insights into evolutionary dynamics under global environmental changes, and are directly applicable to biodiversity conservation.
157 citations
Cites background from "Reproductive asynchrony in natural ..."
...Moreover, asynchrony (and protandry) has been shown to enhance Allee effects in small populations through increased female matelesness (Calabrese et al. 2008)....
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TL;DR: Empirical and experimental studies reporting the probability that some females remain unmated in field populations of insects (defined herein as mating failures) are reviewed in more than 100 species, suggesting a higher mating success in butterflies than moths.
Abstract: Empirical and experimental studies reporting the probability that some females remain unmated in field populations of insects (defined herein as mating failures) are reviewed in more than 100 species. The techniques used to quantify mating failures in the field are summarized, as well as factors that influence the probability that females mate during their lifetime. The existing empirical data provide partial support for hypotheses generated by theoretical models, although the trends observed in field populations are far more diverse and complex than predictions derived from ecological theory, e.g., the effect of population density on female mating success at small and large spatial scales is opposite. Mating success of females increases with the ratio of males in the population, but the relation between emergence time, sex ratio, and female mating success is variable. Females have evolved a broad range of physiological and behavioural adaptations to reduce mating failures, and exhibit a flexible context-dependent response to constraints limiting mating success. The large number of studies in Lepidoptera suggests a higher mating success in butterflies than moths. Examples of high rates of mating failure include species with gynogenous reproduction, long range migration, pre-reproductive maturation, male-biased sex ratio, acquisition of resources essential for reproduction, and female flightlessness. Species with sessile females that mate and oviposit near their emergence site provide model systems to investigate the causes and demographic consequences of female mating failure.
142 citations
Cites background from "Reproductive asynchrony in natural ..."
...…arenosella ER ET Muralimohan & Srinivasa, 2010 Papilionidae Papilio zelicaon SC AGE, HL Shields, 1967; Sims, 1979 Parnassius clodius ER ET Calabrese et al., 2008 Parnassius smintheus ER ET Calabrese et al., 2008 Pieridae Pieris protodice SC PD Shapiro, 1970 Psychidae Metisa plana PMD…...
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...In some species, males deposit a conspicuous mating plug (sphragis) to prevent females from remating, thus allowing non-lethal field assessment (Matsumoto & Suzuki, 1992; Calabrese et al., 2008)....
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...Late emerging females have a low mating success in protandrous populations due to a shortage of males (Higgins, 2000; Calabrese et al., 2008; Muralimohan & Srinivasa, 2010) (Figure 1A)....
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...…2010 Papilionidae Papilio zelicaon SC AGE, HL Shields, 1967; Sims, 1979 Parnassius clodius ER ET Calabrese et al., 2008 Parnassius smintheus ER ET Calabrese et al., 2008 Pieridae Pieris protodice SC PD Shapiro, 1970 Psychidae Metisa plana PMD BS, PD Rhainds et al., 1999 Oiketicus kirbyi PMD…...
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TL;DR: It is far from clear whether polyandry has a net positive or negative effect on female fitness, but it is stressed that its effects on individuals may not have visible demographic consequences and researchers are urged to consider the ecological consequences of evolutionary processes.
Abstract: Polyandry, by elevating sexual conflict and selecting for reduced male care relative to monandry, may exacerbate the cost of sex and thereby seriously impact population fitness. On the other hand, polyandry has a number of possible population-level benefits over monandry, such as increased sexual selection leading to faster adaptation and a reduced mutation load. Here, we review existing information on how female fitness evolves under polyandry and how this influences population dynamics. In balance, it is far from clear whether polyandry has a net positive or negative effect on female fitness, but we also stress that its effects on individuals may not have visible demographic consequences. In populations that produce many more offspring than can possibly survive and breed, offspring gained or lost as a result of polyandry may not affect population size. Such ecological ‘masking’ of changes in population fitness could hide a response that only manifests under adverse environmental conditions (e.g. anthropogenic change). Surprisingly few studies have attempted to link mating system variation to population dynamics, and in general we urge researchers to consider the ecological consequences of evolutionary processes.
112 citations
Cites background from "Reproductive asynchrony in natural ..."
...Since then, much theory has been developed to contrast the population-level consequences of monogamy and multiple mating [2–5], including factors causally underlying mate availability, such as the temporally varying number of males per female [6,7]....
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TL;DR: The simple point that females encounter mates over their lifetime in a stochastic manner is made, and as they should accept at least one male, acceptance of all males may be a better null model than the more advanced strategy of accepting the first satisfactory one and rejecting all others.
Abstract: Why do females of so many species mate multiply? The question makes use of an implicit null model that females by default should be monandrous and that polyandry requires an explanation. Here, we make thesimplepoint that females encountermates overtheir lifetimeina stochasticmanner,andas theyshouldacceptatleastonemale,acceptanceofallmales maybea betternullmodelthanthemore advanced strategy of accepting thefirst satisfactory one and rejecting all others. The advantage of this view is that it makes it explicit that females must accept and reject mates without precise knowledge of future mate encounters. In insects, for example, limitations of cognitive and sensory capabilities make it hard for females to compare many potential mates simultaneously. It is then not always possible for a female to be very choosy (i.e., to reject a large proportion of encounters) without simultaneously increasing the expected time spent as a virgin and decreasing the overall expected number of mates she accrues during her lifetime. We show that this fact easily leads to a pattern where choosiness isreduced and most females mate withmoremales thantheir optimalmate number.Our results suggest that monandry and polyandry may be less distinct strategies than they first appear as they may,toalargeextent,reflectchanceeventsinfluencingmateencounters.Polyandrycanariseasaside effectofavoidingtheriskofencounteringtoofewacceptablemates–a viewpoint that is easilymissed if females that haveremainedunmated arenotincludedindatasets.
79 citations
Cites background from "Reproductive asynchrony in natural ..."
...Fecundity or mortality costs (or direct benefits) of multiple mating, or the fitness consequences of female choice, are much more popular study topics than the risk of never mating (but see de Jong & Sabelis, 1991; Bode & Marshall, 2007; Calabrese et al., 2008; Rhainds, 2010; Elzinga et al., 2011)....
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References
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Book•
19 Jun 2013
TL;DR: The second edition of this book is unique in that it focuses on methods for making formal statistical inference from all the models in an a priori set (Multi-Model Inference).
Abstract: Introduction * Information and Likelihood Theory: A Basis for Model Selection and Inference * Basic Use of the Information-Theoretic Approach * Formal Inference From More Than One Model: Multi-Model Inference (MMI) * Monte Carlo Insights and Extended Examples * Statistical Theory and Numerical Results * Summary
36,993 citations
"Reproductive asynchrony in natural ..." refers methods in this paper
...Finally, we calculate an Akaike-weighted average q* across all submodels (Burnham & Anderson 2002)....
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...For each parameterized c(·) model, we then calculate q* and an Akaike’s information criterion (AIC)-based ranking (Burnham & Anderson 2002), thus allowing a comparison of the effects of different mating factor assumptions, and an indication of which assumptions are best supported by the data....
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Book•
01 Jan 1994
TL;DR: In this paper, a generalized linear model for longitudinal data and transition models for categorical data are presented. But the model is not suitable for categric data and time dependent covariates are not considered.
Abstract: 1. Introduction 2. Design considerations 3. Exploring longitudinal data 4. General linear models 5. Parametric models for covariance structure 6. Analysis of variance methods 7. Generalized linear models for longitudinal data 8. Marginal models 9. Random effects models 10. Transition models 11. Likelihood-based methods for categorical data 12. Time-dependent covariates 13. Missing values in longitudinal data 14. Additional topics Appendix Bibliography Index
7,156 citations
TL;DR: The Allee effect describes a scenario in which populations at low numbers are affected by a positive relationship between population growth rate and density, which increases their likelihood of extinction.
Abstract: The Allee effect describes a scenario in which populations at low numbers are affected by a positive relationship between population growth rate and density, which increases their likelihood of extinction The importance of this dynamic process in ecology has been under-appreciated and recent evidence now suggests that it might have an impact on the population dynamics of many plant and animal species Studies of the causal mechanisms generating Allee effects in small populations could provide a key to understanding their dynamics
1,634 citations
TL;DR: The Allee effect can be regarded not only as a suite of problems associated with rarity, but also as the basis of animal sociality.
Abstract: Warder C. Allee brought attention to the possibility of a positive relationship between aspects of fitness and population size 50 years ago. Until recently, however, this concept was generally regarded as an intriguing but relatively unimportant aspect of population ecology. Increasing appreciation that Allee effects must be incorporated into models of population dynamics and habitat use, together with recent interest in the implications of sociality for conservation, have shown that for ecology and conservation the consequences of the Allee effect are profound. The Allee effect can be regarded not only as a suite of problems associated with rarity, but also as the basis of animal sociality.
1,130 citations