Does past evolutionary history under different mating regimes influence the demographic dynamics of interspecific competition?
ABSTRACT: Interspecific interactions are contingent upon organism phenotypes, and thus phenotypic evolution can modify interspecific interactions and affect ecological dynamics. Recent studies have suggested that male-male competition within a species selects for capability to reproductively interfere with a closely related species. Here, we examine the effect of past evolutionary history under different mating regimes on the demographic dynamics of interspecific competition in Callosobruchus seed beetles. We used previously established experimental evolution lines of Callosobruchus chinensis that evolved under either forced lifelong monogamy or polygamy for 17 generations, and examined the demographic dynamics of competition between these C. chinensis lines and a congener, Callosobruchus maculatus. Callosobruchus chinensis was competitively excluded by C. maculatus in all trials. Time series data analyses suggested that reproductive interference from C. chinensis was relatively more important in the trials involving polygamous C. chinensis than those involving monogamous C. chinensis, in accordance with the potentially higher reproductive interference capability of polygamous C. chinensis. However, the estimated signs and magnitudes of interspecific interactions were not fully consistent with this explanation, implying the evolution of not only reproductive interference but also other interaction mechanisms. Our study thus suggests multifaceted effects of sexually selected traits on interspecific competitive dynamics.
Project description:Interspecific resource competition is expected to select for divergence in resource use, weakening interspecific relative to intraspecific competition, thus promoting stable coexistence. More broadly, because interspecific competition reduces fitness, any mechanism of interspecific competition should generate selection favoring traits that weaken interspecific competition. However, species also can adapt to competition by increasing their competitive ability, potentially destabilizing coexistence. We reared two species of bean beetles, the specialist Callosobruchus maculatus and the generalist C. chinensis, in allopatry and sympatry on a mixture of adzuki beans and lentils, and assayed mutual invasibility after four, eight, and twelve generations of evolution. Contrary to the expectation that coevolution of competitors will weaken interspecific competition, the rate of mutual invasibility did not differ between sympatry and allopatry. Rather, the invasion rate of C. chinensis, but not C. maculatus, increased with duration of evolution, as C. chinensis adapted to lentils without experiencing reduced adaptation to adzuki beans, and regardless of the presence or absence of C. maculatus. Our results highlight that evolutionary responses to interspecific competition promote stable coexistence only under specific conditions that can be difficult to produce in practice.
Project description:Interspecific mating interactions, or reproductive interference, can affect population dynamics, species distribution and abundance. Previous population dynamics models have assumed that the impact of frequency-dependent reproductive interference depends on the relative abundances of species. However, this assumption could be an oversimplification inappropriate for making quantitative predictions. Therefore, a more general model to forecast population dynamics in the presence of reproductive interference is required. Here we developed a population dynamics model to describe the absolute density dependence of reproductive interference, which appears likely when encounter rate between individuals is important. Our model (i) can produce diverse shapes of isoclines depending on parameter values and (ii) predicts weaker reproductive interference when absolute density is low. These novel characteristics can create conditions where coexistence is stable and independent from the initial conditions. We assessed the utility of our model in an empirical study using an experimental pair of seed beetle species, Callosobruchus maculatus and Callosobruchus chinensis. Reproductive interference became stronger with increasing total beetle density even when the frequencies of the two species were kept constant. Our model described the effects of absolute density and showed a better fit to the empirical data than the existing model overall.
Project description:Zombi pea (Vigna vexillata) is a legume crop that is resistant to several biotic and abiotic stresses. Callosobruchus maculatus and Callosobruchus chinensis are serious stored-insect pests of legume crops. We constructed a high-density linkage map and performed quantitative trait loci (QTLs) mapping for resistance to these insect species in zombi pea. An F2 population of 198 individuals from a cross between 'TVNu 240' (resistant) and 'TVNu 1623' (susceptible) varieties was used to construct a linkage map of 6,529 single nucleotide polymorphism markers generated from sequencing amplified fragments of specific loci. The map comprised 11 linkage groups, spanning 1,740.9 cM, with an average of 593.5 markers per linkage group and an average distance of 0.27 cM between markers. High levels of micro-synteny between V. vexillata and cowpea (Vigna unguiculata), mungbean (Vigna radiata), azuki bean (Vigna angularis) and common bean (Phaseolus vulgaris) were found. One major and three minor QTLs for C. chinensis resistance and one major and one minor QTLs for C. maculatus resistance were identified. The major QTLs for resistance to C. chinensis and C. maculatus appeared to be the same locus. The linkage map developed in this study will facilitate the identification of useful genes/QTLs in zombi pea.
Project description:Theory maintains within-group male relatedness can mediate sexual conflict by reducing male-male competition and collateral harm to females. We tested whether male relatedness can lessen female harm in the seed beetle Callosobruchus maculatus. Male relatedness did not influence female lifetime reproductive success or individual fitness across two different ecologically relevant scenarios of mating competition. However, male relatedness marginally improved female survival. Because male relatedness improved female survival in late life when C. maculatus females are no longer producing offspring, our results do not provide support for the role of within-group male relatedness in mediating sexual conflict. The fact that male relatedness improves the post-reproductive part of the female life cycle strongly suggests that the effect is non-adaptive. We discuss adaptive and non-adaptive mechanisms that could result in reduced female harm in this and previous studies, and suggest that cognitive error is a likely explanation.
Project description:Ecological theory suggests that frequency-dependent predation, in which more common prey types are disproportionately favored, promotes the coexistence of competing prey species. However, many of the earlier empirical studies that investigated the effect of frequency-dependent predation were short-term and ignored predator-prey dynamics and system persistence. Therefore, we used long-term observation of population dynamics to test how frequency-dependent predation influences the dynamics and coexistence of competing prey species using insect laboratory populations. We established two-host-one-parasitoid populations with two bruchid beetles, Callosobruchus chinensis and C. maculatus, as the hosts and the pteromalid wasp Anisopteromalus calandrae as their common parasitoid. When the parasitoid was absent, C. chinensis was competitively excluded in ?20 wk. Introducing the parasitoid greatly enhanced the coexistence time to a maximum of 118 wk. In the replicates of long-lasting coexistence, the two host species C. maculatus and C. chinensis exhibited periodic antiphase oscillations. Behavioral experiments showed frequency-dependent predation of A. calandrae that was caused by learning. Females of A. calandrae learned host-related olfactory cues during oviposition and increased their preference for the common host species. Numerical simulations showed that parasitoid learning was the essential mechanism that promoted persistence in this host-parasitoid system. Our study is an empirical demonstration that frequency-dependent predation has an important role in greatly enhancing the coexistence of prey populations, suggesting that predator learning affects predator-prey population dynamics and shapes biological communities in nature.
Project description:Nearly all mungbean cultivars are completely susceptible to seed bruchids (Callosobruchus chinensis and Callosobruchus maculatus). Breeding bruchid-resistant mungbean is a major goal in mungbean breeding programs. Recently, we demonstrated in mungbean (Vigna radiata) accession V2802 that VrPGIP2, which encodes a polygalacturonase inhibiting protein (PGIP), is the Br locus responsible for resistance to C. chinensis and C. maculatus. In this study, mapping in mungbean accession V2709 using a BC11F2 population of 355 individuals revealed that a single major quantitative trait locus, which controlled resistance to both C. chinensis and C. maculatus, was located in a 237.35 Kb region of mungbean chromosome 5 that contained eight annotated genes, including VrPGIP1 (LOC106760236) and VrPGIP2 (LOC106760237). VrPGIP1 and VrPGIP2 are located next to each other and are only 27.56 Kb apart. Sequencing VrPGIP1 and VrPGIP2 in "V2709" revealed new alleles for both VrPGIP1 and VrPGIP2, named VrPGIP1-1 and VrPGIP2-2, respectively. VrPGIP2-2 has one single nucleotide polymorphism (SNP) at position 554 of wild type VrPGIP2. This SNP is a guanine to cystine substitution and causes a proline to arginine change at residue 185 in the VrPGIP2 of "V2709". VrPGIP1-1 has 43 SNPs compared with wild type and "V2802", and 20 cause amino acid changes in VrPGIP1. One change is threonine to proline at residue 185 in VrPGIP1, which is the same as in VrPGIP2. Sequence alignments of VrPGIP2 and VrPGIP1 from "V2709" with common bean (Phaseolus vulgaris) PGIP2 revealed that residue 185 in VrPGIP2 and VrPGIP1 contributes to the secondary structures of proteins that affect interactions between PGIP and polygalacturonase, and that some amino acid changes in VrPGIP1 also affect interactions between PGIP and polygalacturonase. Thus, tightly linked VrPGIP1 and VrPGIP2 are the likely genes at the Br locus that confer bruchid resistance in mungbean "V2709".
Project description:Across the animal kingdom the duration of copulation varies enormously from a few seconds to several days. Functional explanations for this variation are largely embedded within sperm competition theory in which males modulate the duration of copula in order to optimize their fitness. However, copulation is the union of two protagonists which are likely to have separate and often conflicting reproductive interests, yet few experimental designs specifically assess the effect of male-female interactions on the duration of copulation. This can result in inexact assertions over which sex controls copulatory behaviour. Here we analyse the repeatability of copulatory behaviour in the seed beetle Callosobruchus maculatus to determine which sex exerts primary influence over copulation duration. In C. maculatus, copulation follows two distinct phases: an initial quiescent phase followed by a period of vigorous female kicking behaviour that culminates in the termination of copulation. When males or females copulated with several novel mates, copulatory behaviour was not significantly repeatable. By contrast, when males or females mated repeatedly with the same mate, copula duration was repeatable. These data suggest copulatory behaviour in C. maculatus to be largely the product of male-female interactions rather than the consistent, sex-specific modulation of copula duration of one protagonist in response to the phenotypic variation presented by the other protagonist.
Project description:Genetic variation in dispersal ability may result in the spatial sorting of alleles during range expansion. Recent theory suggests that spatial sorting can favour the rapid evolution of life history traits at expanding fronts, and therefore modify the ecological dynamics of range expansion. Here we test this prediction by disrupting spatial sorting in replicated invasions of the bean beetle Callosobruchus maculatus across homogeneous experimental landscapes. We show that spatial sorting promotes rapid evolution of dispersal distance, which increases the speed and variability of replicated invasions: after 10 generations of range expansion, invasions subject to spatial sorting spread 8.9% farther and exhibit 41-fold more variable spread dynamics relative to invasions in which spatial sorting is suppressed. Correspondingly, descendants from spatially evolving invasions exhibit greater mean and variance in dispersal distance. Our results reveal an important role for rapid evolution during invasion, even in the absence of environmental filters, and argue for evolutionarily informed forecasts of invasive spread by exotic species or climate change migration by native species.
Project description:Males of many species adjust their reproductive investment to the number of rivals present simultaneously. However, few studies have investigated whether males sum previous encounters with rivals, and the total level of competition has never been explicitly separated from social familiarity. Social familiarity can be an important component of kin recognition and has been suggested as a cue that males use to avoid harming females when competing with relatives. Previous work has succeeded in independently manipulating social familiarity and relatedness among rivals, but experimental manipulations of familiarity are confounded with manipulations of the total number of rivals that males encounter. Using the seed beetle Callosobruchus maculatus, we manipulated three factors: familiarity among rival males, the maximum number of rivals encountered simultaneously and the total number of rivals encountered over a 48 h period. Males produced smaller ejaculates when exposed to more rivals in total, regardless of the maximum number of rivals they encountered simultaneously. Males did not respond to familiarity. Our results demonstrate that males of this species can sum the number of rivals encountered over separate days, and therefore the confounding of familiarity with the total level of competition in previous studies should not be ignored.
Project description:Mitochondrial DNA (mtDNA) consists of few but vital maternally inherited genes that interact closely with nuclear genes to produce cellular energy. How important mtDNA polymorphism is for adaptation is still unclear. The assumption in population genetic studies is often that segregating mtDNA variation is selectively neutral. This contrasts with empirical observations of mtDNA haplotypes affecting fitness-related traits and thermal sensitivity, and latitudinal clines in mtDNA haplotype frequencies. Here, we experimentally test whether ambient temperature affects selection on mtDNA variation, and whether such thermal effects are influenced by intergenomic epistasis due to interactions between mitochondrial and nuclear genes, using replicated experimental evolution in Callosobruchus maculatus seed beetle populations seeded with a mixture of different mtDNA haplotypes. We also test for sex-specific consequences of mtDNA evolution on reproductive success, given that mtDNA mutations can have sexually antagonistic fitness effects. Our results demonstrate natural selection on mtDNA haplotypes, with some support for thermal environment influencing mtDNA evolution through mitonuclear epistasis. The changes in male and female reproductive fitness were both aligned with changes in mtDNA haplotype frequencies, suggesting that natural selection on mtDNA is sexually concordant in stressful thermal environments. We discuss the implications of our findings for the evolution of mtDNA.