Reproductive Success In Natural Populations Research Articles

The multinomial index: a robust measure of reproductive skew.

Inequality or skew in reproductive success (RS) is common across many animal species and is of long-standing interest to the study of social evolution. However, the measurement of inequality in RS in natural populations has been challenging because existing quantitative measures are highly sensitive to variation in group/sample size, mean RS, and age-structure. This makes comparisons across multiple groups and/or species vulnerable to statistical artefacts and hinders empirical and theoretical progress. Here, we present a new measure of reproductive skew, the multinomial index, M, that is unaffected by many of the structural biases affecting existing indices. M is analytically related to Nonacs’ binomial index, B, and comparably accounts for heterogeneity in age across individuals; in addition, M allows for the possibility of diminishing or even highly nonlinear RS returns to age. Unlike B, however, M is not biased by differences in sample/group size. To demonstrate the value of our index for cross-population comparisons, we conduct a reanalysis of male reproductive skew in 31 primate species. We show that a previously reported negative effect of group size on mating skew was an artefact of structural biases in existing skew measures, which inevitably decline with group size; this bias disappears when using M. Applying phylogenetically controlled, mixed-effects models to the same dataset, we identify key similarities and differences in the inferred within- and between-species predictors of reproductive skew across metrics. Finally, we provide an R package, SkewCalc, to estimate M from empirical data.

RNA-Seq and differential gene expression analysis in Temora stylifera copepod females with contrasting non-feeding nauplii survival rates: an environmental transcriptomics study

BackgroundCopepods are fundamental components of pelagic food webs, but reports on how molecular responses link to reproductive success in natural populations are still scarce. We present a de novo transcriptome assembly and differential expression (DE) analysis in Temora stylifera females collected in the Gulf of Naples, Mediterranean Sea, where this copepod dominates the zooplankton community. High-Throughput RNA-Sequencing and DE analysis were performed from adult females collected on consecutive weeks (May 23rd and 30th 2017), because opposite naupliar survival rates were observed. We aimed at detecting key genes that may have influenced copepod reproductive potential in natural populations and whose expression was potentially affected by phytoplankton-derived oxylipins, lipoxygenase-derived products strongly impacting copepod naupliar survival.ResultsOn the two sampling dates, temperature, salinity, pH and oxygen remained stable, while variations in phytoplankton cell concentration, oxylipin concentration and oxylipin-per-diatom-cell production were observed. T. stylifera naupliar survival was 25% on May 23rd and 93% on May 30th. De novo assembly generated 268,665 transcripts (isoforms) and 120,749 unique ‘Trinity predicted genes’ (unigenes), of which 50% were functionally annotated. Out of the 331 transcript isoforms differentially expressed between the two sampling dates, 119 sequences were functionally annotated (58 up- and 61 down-regulated). Among predicted genes (unigenes), 144 sequences were differentially expressed and 31 (6 up-regulated and 25 down-regulated) were functionally annotated. Most of the significantly down-regulated unigenes and isoforms were A5 Putative Odorant Binding Protein (Obp). Other differentially expressed sequences (isoforms and unigenes) related to developmental metabolic processes, protein ubiquitination, response to stress, oxidation-reduction reactions and hydrolase activities. DE analysis was validated through Real Time-quantitative PCR of 9 unigenes and 3 isoforms.ConclusionsDifferential expression of sequences involved in signal detection and transduction, cell differentiation and development offered a functional interpretation to the maternally-mediated low naupliar survival rates observed in samples collected on May 23rd. Down-regulation of A5 Obp along with higher quantities of oxylipins-per-litre and oxylipins-per-diatom-cell observed on May 23rd could suggest oxylipin-mediated impairment of naupliar survival in natural populations of T. stylifera. Our results may help identify biomarker genes explaining variations in copepod reproductive responses at a molecular level.

Genetic evidence for alloparental care and frequent multiple paternity in the brooding sea star (Leptasterias sp.)

Echinoderms form an abundant and ecologically important group of marine animals, and they are found in nearly every marine environment, from shallow tropical waters to deep polar benthos and even in the pelagic zone. They exhibit a wide diversity of reproductive strategies that range from broadcasting millions of gametes, with no parental care, to internal brooding of a few embryos for several weeks. While many echinoderm species have become model systems for studies of community ecology, evolutionary genetics, and development biology, very little is known about the distribution of mating and reproductive success in natural populations. In this study, we examined patterns of genetic maternity and paternity in the six-rayed sea star Leptasterias sp., an important predator of many intertidal communities and a species that exhibits maternal care of embryos. We used next-generation sequencing to rapidly develop informative microsatellite markers for this species, and used these markers to genotype 439 juveniles across 15 broods collected from the intertidal in Fogarty Creek, Oregon, USA. Our data show an unambiguous pattern of multiple paternity in all but one clutch examined, with some broods showing some of the highest levels of polyandry reported for a marine invertebrate. Moreover, we detected two cases of mixed maternity in which a female sea star carried another mother’s offspring mixed with her own. Alloparental care by females is rare, and since female Leptasterias do not eat during the 40–60 days brooding period, this expensive behavior may provide a useful system for examining the evolutionary costs and benefits of parental care in dynamic intertidal environments.

Reproductive success through high pollinator visitation rates despite self incompatibility in an endangered wallflower.

Self incompatibility (SI) in rare plants presents a unique challenge-SI protects plants from inbreeding depression, but requires a sufficient number of mates and xenogamous pollination. Does SI persist in an endangered polyploid? Is pollinator visitation sufficient to ensure reproductive success? Is there evidence of inbreeding/outbreeding depression? We characterized the mating system, primary pollinators, pollen limitation, and inbreeding/outbreeding depression in Erysimum teretifolium to guide conservation efforts. We compared seed production following self pollination and within- and between-population crosses. Pollen tubes were visualized after self pollinations and between-population pollinations. Pollen limitation was tested in the field. Pollinator observations were quantified using digital video. Inbreeding/outbreeding depression was assessed in progeny from self and outcross pollinations at early and later developmental stages. Self-pollination reduced seed set by 6.5× and quadrupled reproductive failure compared with outcross pollination. Pollen tubes of some self pollinations were arrested at the stigmatic surface. Seed-set data indicated strong SI, and fruit-set data suggested partial SI. Pollinator diversity and visitation rates were high, and there was no evidence of pollen limitation. Inbreeding depression (δ) was weak for early developmental stages and strong for later developmental stages, with no evidence of outbreeding depression. The rare hexaploid E. teretifolium is largely self incompatible and suffers from late-acting inbreeding depression. Reproductive success in natural populations was accomplished through high pollinator visitation rates consistent with a lack of pollen limitation. Future reproductive health for this species will require large population sizes with sufficient mates and a robust pollinator community.

Reproductive interference between Rana dalmatina and Rana temporaria affects reproductive success in natural populations.

Experimental evidence suggests that reproductive interference between heterospecifics can seriously affect individual fitness; support from field studies for such an effect has, however, remained scarce. We studied reproductive interference in 25 natural breeding ponds in an area where two ranid frogs, Rana dalmatina and Rana temporaria, co-occur. The breeding seasons of the two species usually overlap and males of both species are often found in amplexus with heterospecific females, even though matings between heterospecifics produce no viable offspring. We estimated species abundance ratios based on the number of clutches laid and evaluated fertilization success. In ponds with low spatial complexity and a species abundance ratio biased towards R. temporaria, the average fertilization success of R. dalmatina eggs decreased, while this relationship was not detectable in spatially more complex ponds. Fertilization success of R. temporaria did not decrease with increasing relative numbers of heterospecifics. This asymmetry in fitness effects of reproductive interference may be attributed to R. temporaria males being more competitive in scramble competition for females than R. dalmatina males. Our study is among the first to demonstrate that in natural breeding populations of vertebrates interference among heterospecifics has the potential to substantially lower reproductive success at the population level, which may in turn affect population dynamics.

Positive effect of the yellow morph on female reproductive success in the flower colour polymorphic Iris lutescens (Iridaceae), a deceptive species.

The deceptive Iris lutescens (Iridaceae) shows a heritable and striking flower colour polymorphism, with both yellow- and purple-flowered individuals growing sympatrically. Deceptive species with flower colour polymorphism are mainly described in the family Orchidaceae and rarely found in other families. To explain the maintenance of flower colour polymorphism in I.lutescens, we investigated female reproductive success in natural populations of southern France, at both population and local scales (within populations). Female reproductive success was positively correlated with yellow morph frequency, at both the population scale and the local scale. Therefore, we failed to observe negative frequency-dependent selection (NFDS), a mechanism commonly invoked to explain flower colour polymorphism in deceptive plant species. Flower size and local flower density could also affect female reproductive success in natural populations. Pollinator behaviour could explain the positive effect of the yellow morph, and our results suggest that flower colour polymorphism might not persist in I.lutescens, but alternative explanations not linked to pollinator behaviour are discussed. In particular, NFDS, although an appealingly simple explanation previously demonstrated in orchids, may not always contribute to maintaining flower colour polymorphism, even in deceptive species.

Parental genetic distance and patterns in nonrandom mating and seed yield in predominately selfing Arabidopsis thaliana

In this study, we ask two questions: (1) Is reproductive success independent of parental genetic distance in predominately selfing plants? (2) In the absence of early inbreeding depression, is there substantial maternal and/or paternal variation in reproductive success in natural populations? Seed yield in single pollinations and proportion of seeds sired in mixed pollinations were studied in genetically defined accessions of the predominately selfing plant Arabidopsis thaliana by conducting two diallel crosses. The first diallel was a standard, single pollination design that we used to examine variance in seed yield. The second diallel was a mixed pollination design that utilized a standard pollen competitor to examine variance in proportion of seeds sired. We found no correlation between reproductive success and parental genetic distance, and self-pollen does not systematically differ in reproductive success compared to outcross pollen, suggesting that Arabidopsis populations do not experience embryo lethality due to early-acting inbreeding or outbreeding depression. We used these data to partition the contributions to total phenotypic variation from six sources, including maternal contributions, paternal contributions and parental interactions. For seed yield in single pollinations, maternal effects accounted for the most significant source of variance (16.6 %). For proportion of seeds sired in mixed pollinations, the most significant source of variance was paternal effects (17.9 %). Thus, we show that population-level genetic similarities, including selfing, do not correlate with reproductive success, yet there is still significant paternal variance under competition. This suggests two things. First, since these differences are unlikely due to early-acting inbreeding depression or differential pollen viability, this implicates natural variation in pollen germination and tube growth dynamics. Second, this strongly supports a model of fixation of pollen performance genes in populations, offering a focus for future genetic studies in differential reproductive success.

Genetic Diversity in Cytokines Associated with Immune Variation and Resistance to Multiple Pathogens in a Natural Rodent Population

Pathogens are believed to drive genetic diversity at host loci involved in immunity to infectious disease. To date, studies exploring the genetic basis of pathogen resistance in the wild have focussed almost exclusively on genes of the Major Histocompatibility Complex (MHC); the role of genetic variation elsewhere in the genome as a basis for variation in pathogen resistance has rarely been explored in natural populations. Cytokines are signalling molecules with a role in many immunological and physiological processes. Here we use a natural population of field voles (Microtus agrestis) to examine how genetic diversity at a suite of cytokine and other immune loci impacts the immune response phenotype and resistance to several endemic pathogen species. By using linear models to first control for a range of non-genetic factors, we demonstrate strong effects of genetic variation at cytokine loci both on host immunological parameters and on resistance to multiple pathogens. These effects were primarily localized to three cytokine genes (Interleukin 1 beta (Il1b), Il2, and Il12b), rather than to other cytokines tested, or to membrane-bound, non-cytokine immune loci. The observed genetic effects were as great as for other intrinsic factors such as sex and body weight. Our results demonstrate that genetic diversity at cytokine loci is a novel and important source of individual variation in immune function and pathogen resistance in natural populations. The products of these loci are therefore likely to affect interactions between pathogens and help determine survival and reproductive success in natural populations. Our study also highlights the utility of wild rodents as a model of ecological immunology, to better understand the causes and consequences of variation in immune function in natural populations including humans.

Variance in the reproductive success of flat oysterOstrea edulisL. assessed by parentage analyses in natural and experimental conditions

In order to document further the phenomena of variance in reproductive success in natural populations of the European flat oyster Ostrea edulis, two complementary studies based on natural and experimental populations were conducted. The first part of this work was focused on paternity analyses using a set of four microsatellite markers for larvae collected from 13 brooding females sampled in Quiberon Bay (Brittany, France). The number of individuals contributing as the male parent to each progeny assay was highly variable, ranging from 2 to more than 40. Moreover, paternal contributions showed a much skewed distribution, with some males contributing to 50-100% of the progeny assay. The second part of this work consisted of the analysis of six successive cohorts experimentally produced from an acclimated broodstock (62 wild oysters sampled in the Quiberon Bay). Allelic richness was significantly higher in the adult population than in the temporal cohorts collected. Genetic differentiation (F(st) estimates) was computed for each pair of samples and all significant values ranged from 0.7 to 11.9%. A limited effective number of breeders (generally below 25) was estimated in the six temporal cohorts. The study gives first indications of the high variance in reproductive success as well as a reduced effective size, not only under experimental conditions but also in the wild. Surprisingly, the pool of the successive cohorts, based on the low number of loci used, appeared to depict a random and representative set of alleles of the progenitor population, indicating that the detection of patterns of temporal genetic differentiation at a local scale most likely depends on the sampling window.

Fragment size, pollination efficiency and reproductive success in natural populations of wind-pollinated Polylepis australis (Rosaceae) trees

It is well known that habitat fragmentation is likely to negatively affect the reproductive success of a species. Despite this fact, studies on the effects of fragmentation on reproductive success in combination with effects on natural pollination of wind-pollinated tree species are very rare. In this study, we analyzed the relationships between fragment size, components of pollination efficiency, reproductive success and progeny vigour of the highly fragmented populations of the wind-pollinated treeline species Polylepis australis (Rosaceae) in Argentina. We conducted our study in the high mountains of Córdoba, comparing pollination efficiency and reproduction between four fragment sizes. Most of our results indicate that P. australis is currently insensitive to fragmentation. However, our study revealed also a linear increase in leaf area and biomass of 40-day-old seedlings with increasing fragment size. Inbreeding problems through fragmentation as well as decreased habitat quality in small fragments are discussed as possible causes for the impaired progeny vigour.

Multiple paternity in wild‐caughtDrosophila mojavensis

Female remating frequency and sperm allocation patterns can strongly influence levels of sperm competition and reproductive success in natural populations. In the laboratory, Drosophila mojavensis males transfer very few sperm per copulation and females remate often, suggesting multiple paternity should be common in nature. Here, we examine female sperm loads, incidence of multiple paternity, and sperm utilization by genotyping progeny from 20 wild-caught females at four highly polymorphic microsatellite loci. Based on indirect paternity analyses of 814 flies, we found evidence for high levels of multiple paternity coupled with relatively low reproductive output, consistent with the high levels of female remating predicted in this sperm-limited species. Overall, we found little evidence for last -- male sperm precedence though some temporal variation in sperm utilization was observed, consistent with laboratory findings.

MINIMAL SELFING, FEW CLONES, AND NO AMONG‐HOST GENETIC STRUCTURE IN A HERMAPHRODITIC PARASITE WITH ASEXUAL LARVAL PROPAGATION

Little is known about actual mating systems in natural populations of parasites or about what constitutes the limits of a parasite deme. These parameters are interesting because they affect levels of genetic diversity, opportunities for local adaptation, and other evolutionary processes. We expect that transmission dynamics and the distribution of parasites among hosts should have a large effect on mating systems and demic structure, but currently we have mostly speculation and very few data. For example, infrapopulations (all the parasites in a single host) should behave as demes if parasite offspring are transmitted as a clump from host to host over several generations. However, if offspring are well mixed, then the parasite component population (all the parasites among a host population) would function as the deme. Similarly, low mean intensities or a high proportion of worms in single infections should increase the selfing rate. For species having an asexual amplification stage, transmission between intermediate and definitive (final) hosts will control the variance in clonal reproductive success, which in turn could have a large influence on effective sizes and rates of inbreeding. We examined demic structure, selfing rates, and the variance in clonal reproductive success in natural populations of Plagioporus shawi, a hermaphroditic trematode that parasitizes salmon. Overall levels of genetic diversity were very high. An a posteriori inference of population structure overwhelmingly supports the component population as the deme, rather than individual infrapopulations. Only a single pair of 597 adult individuals was identified as clones. Thus, the variance in clonal reproductive success was almost zero. Despite being hermaphroditic, P. shawi appears to be almost entirely outcrossing. Genetic estimates of selfing (<5%) were in accordance with the proportion of parasites from single infections. Thus, it appears that individual flukes outcross whenever possible and only resort to selfing when alone. Finally, our data support the hypothesis that aquatic transmission and the use of several intermediate hosts promotes high genetic diversity and well-mixed infrapopulations.

Forest fragmentation and plant reproductive success: a case study in four perennial herbs

We assessed the effects of habitat fragmentation on reproductive success in natural populations of four forest herbs with differing life-history traits and whose distribution patterns appeared to be negatively affected by decreased habitat size and/or increased isolation: Carex sylvatica, Galium odoratum, Sanicula europaea and Veronica montana. Our aims were to test (1) whether habitat size and isolation are positively correlated with population size and isolation, respectively, (2) whether plant reproductive success, a major component of plant fitness, is reduced in small and/or isolated populations when also accounting for differences in habitat quality (edaphic conditions, light intensity) and the effects of plant size, and (3) whether species with different life histories are affected differently. There were significant positive relationships between habitat and population size and between habitat and population isolation in some, but not all of the species. We mostly found no negative effects of small population size or isolation on reproduction. However, reproductive success was reduced in small populations of Sanicula, and this effect was independent of differences in plant size and environmental conditions. The reduced fecundity in small populations may be a consequence of the Allee-effect, a possible mechanism being pollen limitation. Furthermore, the proportion of flowering ramets was reduced in small and isolated populations of Galium, which may have been caused by changes in population structure. Lastly, we found some evidence for largely outcrossing, non-clonal species to be more sensitive to reductions in population size, at least in terms of their reproductive success.

Patterns in Male Breeding Behaviors in the Bluefin Killifish,Lucania goodei: A Field Study (Cyprinodontiformes: Fundulidae)

Abstract The determinants of male reproductive success in natural populations have not been measured for any fundulid species in North America. In this study, spawnings, courtship of females, and aggression toward other males, females, and heterospecifics were recorded during daylight hours in a natural population of bluefin killifish, Lucania goodei. Three main findings emerge. First, spawning success is correlated with male aggression toward other males and with male courtship of females, indicating that both male/male competition and female choice are likely to be operating. This result implies that both male/male competition and female choice must be considered in studies of sexual selection (as opposed to dichtomous choice tests, which preclude male/male competition). Second, males exhibited substantial levels of aggression toward both nonbreeding females and heterospecifics. Males may be guarding eggs, guarding food items, or trying to keep an open area around them so that they can be seen by gravid...

Evolution and maintenance of stigma-height dimorphism in Narcissus. II. Fitness comparisons between style morphs.

Populations of the insect-pollinated geophytes Narcissus assoanus and N. dubius (Amaryllidaceae) are commonly dimorphic for stigma height. An extensive survey of populations of the two species in SW France revealed a wide range of style-morph frequencies, particularly populations with significantly more long-styled than short-styled plants. Here we employ experimental and theoretical approaches to investigate potential selective mechanisms governing the variation in style-morph frequencies. Controlled pollination of both species demonstrated that N. assoanus is moderately self-sterile whereas N. dubius is highly self-compatible. Both intra- and intermorph crosses of N. assoanus were equally fertile, indicating that the species does not exhibit heteromorphic incompatibility. Estimates of female fertility (fruit- and seed-set) and multilocus estimates of outcrossing using allozyme markers provided no evidence of morph-specific differences in maternal components of reproductive success in natural populations of the two species. This result suggested that differences between the morphs in male fertility may be largely responsible for the observed morph-ratio variation. To investigate this hypothesis we developed a mating model that incorporates the genetics of stigma-height dimorphism and contrasting rates of assortative and disassortative mating in the style morphs. Simulation results demonstrated that stigma-height dimorphism will always be maintained when levels of disassortative mating are greater than assortative mating, and that the observed L-biased populations in Narcissus spp. probably result from greater levels of assortative mating in this morph in comparison with the S-morph.

MHC variation in birds and reptiles.

The major histocompatibility complex (MHC) has been studied in a multitude of mammals by now, but much less is known about its organisation and variation in other vertebrate species. The mammalian MHC is organised as a single gene cluster, but recent studies on birds suggest that this paradigm of MHC organisation has to be supplemented. The domestic chicken thus possesses two separate gene clusters which both contain MHC class I and class II B genes, and we have shown that the ring-necked pheasant Phasianus colchicus also has two unlinked clusters of class II B genes. We are studying the effect of the MHC on mate choice, survival and reproductive success in natural populations of birds and reptiles. For this reason, we are developing DNA techniques to determine the animals' MHC genotype. The amplification of the hypervariable exon 3 of the class I gene from songbirds and reptiles has provided us with species specific probes that can be used in Southern blot analysis. The first results indicate very extensive variation in all studied species, that is starlings Sturnus vulgaris, great reed warblers Acrocephalus arundinaceus and water pythons Liasis fuscus. The restriction fragment length polymorphism (RFLP) analysis also suggests that the number of MHC genes is significantly larger in these species than in pheasants and domestic chickens.

The effect of male size and operational sex ratio on male mating success in the common spider mite, Tetranychus urticae Koch (Acari: Tetranychidae)

Abstract. The effect of male size and operational sex ratio (number of adult males/number of adult males + number of females available for mating) on male mating success in the spider mite was studied both in the field and in the laboratory. Larger males defended females less intensely and for shorter periods, but had a higher probability of mating with a previously guarded female than smaller males. With increasing operational sex ratio agonistic interactions between males occurred more frequently and lasted longer. Large males guarded more selectively, i.e. spent less time guarding, than small ones. With increasing density of quiescent females (females in the final juvenile stage) all mates became more selective. Only small males guarded less selectively with increasing male bias. Females mated repeatedly. A female's first mating lasted longer on average than subsequent matings. In the absence of male-male competition, absolute mate size was positively correlated with the duration of the first mating. When males competed for females, the larger males were better able to resist attempted interference in mating than smaller males. Compared with balanced or female-biased operational sex ratios, mating interferences tended to be more common, although not significantly so, when the operational sex ratio was biased towards males. A male's chance to mate twice with a given female decreased with increasing operational sex ratio. Depending on the degree of male-male competition in a spider mite colony, the effects of male size on fighting ability, chance to mate, duration of precopulatory mate guarding and duration of mating will contribute to variation in male reproductive success in natural populations.