Reproductive inequality in humans and other mammals.

To address claims of human exceptionalism, we determine where humans fit within the greater mammalian distribution of reproductive inequality. We show that humans exhibit lower reproductive skew (i.e., inequality in the number of surviving offspring) among males and smaller sex differences in reproductive skew than most other mammals, while nevertheless falling within the mammalian range. Additionally, female reproductive skew is higher in polygynous human populations than in polygynous nonhumans mammals on average. This patterning of skew can be attributed in part to the prevalence of monogamy in humans compared to the predominance of polygyny in nonhuman mammals, to the limited degree of polygyny in the human societies that practice it, and to the importance of unequally held rival resources to women's fitness. The muted reproductive inequality observed in humans appears to be linked to several unusual characteristics of our species-including high levels of cooperation among males, high dependence on unequally held rival resources, complementarities between maternal and paternal investment, as well as social and legal institutions that enforce monogamous norms.

Parallel evolution of morphological and genomic selfing syndromes accompany the breakdown of heterostyly.

Evolutionary transitions from outcrossing to selfing in flowering plants have convergent morphological and genomic signatures and can involve parallel evolution within related lineages. Adaptive evolution of morphological traits is often assumed to evolve faster than nonadaptive features of the genomic selfing syndrome. We investigated phenotypic and genomic changes associated with transitions from distyly to homostyly in the Primula oreodoxa complex. We determined whether the transition to selfing occurred more than once and investigated stages in the evolution of morphological and genomic selfing syndromes using 22 floral traits and both nuclear and plastid genomic data from 25 populations. Two independent transitions were detected representing an earlier and a more recently derived selfing lineage. The older lineage exhibited classic features of the morphological and genomic selfing syndrome. Although features of both selfing syndromes were less developed in the younger selfing lineage, they exhibited parallel development with the older selfing lineage. This finding contrasts with the prediction that some genomic changes should lag behind adaptive changes to morphological traits. Our findings highlight the value of comparative studies on the timing and extent of transitions from outcrossing to selfing between related lineages for investigating the tempo of morphological and molecular evolution.

Anthropogenic land-use change decreases pollination and male and female fitness in terrestrial flowering plants.

BACKGROUND AND AIMS: The majority of the earth's land area is currently occupied by humans. Measuring how terrestrial plants reproduce in these pervasive environments is essential for understanding their long-term viability and their ability to adapt to changing environments. METHODS: We conducted hierarchical and phylogenetically-independent meta-analyses to assess the overall effects of anthropogenic land-use changes on pollination, and male and female fitness in terrestrial plants. KEY RESULTS: We found negative global effects of land use change (i.e., mainly habitat loss and fragmentation) on pollination and on female and male fitness of terrestrial flowering plants. Negative effects were stronger in plants with self-incompatibility (SI) systems and pollinated by invertebrates, regardless of life form and sexual expression. Pollination and female fitness of pollination generalist and specialist plants were similarly negatively affected by land-use change, whereas male fitness of specialist plants showed no effects. CONCLUSIONS: Our findings indicate that angiosperm populations remaining in fragmented habitats negatively affect pollination, and female and male fitness, which will likely decrease the recruitment, survival, and long-term viability of plant populations remaining in fragmented landscapes. We underline the main current gaps of knowledge for future research agendas and call out not only for a decrease in the current rates of land-use changes across the world but also to embark on active restoration efforts to increase the area and connectivity of remaining natural habitats.

Pollinator foraging tactics have divergent consequences for the mating system of a tropical plant.

Resolving the consequences of pollinator foraging behaviour for plant mating systems is a fundamental challenge in evolutionary ecology. Pollinators may adopt particular foraging tactics: complete trapline foraging (repeated movements along a fixed route), sample-and-shift trapline foraging (a variable route that incorporates information from previous experiences) and territorial foraging (stochastic movements within a restricted area). Studies that integrate these pollinator foraging tactics with plant mating systems are generally lacking. We investigate the consequences of particular pollinator foraging tactics for Heliconia tortuosa. We combine parentage and sibship inference analysis with simulation modelling to: estimate mating system parameters; infer the foraging tactic adopted by the pollinators; and quantify the impact of pollinator foraging tactics on mating system parameters. We found high outcrossing rates, ubiquitous multiple paternity and a pronounced departure from near-neighbour mating. We also found that plants repeatedly receive pollen from a series of particular donors. We infer that the pollinators primarily adopt complete trapline foraging and occasionally engage in sample-and-shift trapline foraging. This enhances multiple paternity without a substantial increase in near-neighbour mating. The particular pollinator foraging tactics have divergent consequences for multiple paternity and near-neighbour mating. Thus, pollinator foraging behaviour is an important driver of the ecology and evolution of plant mating systems.

Comparative floral development in male and female plants of Palmer amaranth (Amaranthus palmeri).

PREMISE: Characterizing the developmental processes in the transition from hermaphroditism to unisexuality is crucial for understanding floral evolution. Amaranthus palmeri, one of the most devastating weeds in the United States, is an emerging model system for studying a dioecious breeding system and understanding the biological traits of this invasive weed. The objectives of this study were to characterize phases of flower development in A. palmeri and compare organogenesis of flower development in female and male plants. METHODS: Flower buds from male and female plants were dissected for light microscopy. Segments of male and female inflorescences at different stages of development were cut longitudinally and visualized using scanning electron microscopy. RESULTS: Pistillate flowers have two to three styles, one ovary with one ovule, and five obtuse tepals. Staminate flowers have five stamens with five acute tepals. Floral development was classified into 10 stages. The distinction between the two flower types became apparent at stage four by the formation of stamen primordia in staminate flowers, which developed female and male reproductive organs initially, as contrasted to pistillate flowers, which produced carpel primordia only. In staminate flowers, the putative carpel primordia changed little in size and remained undeveloped. CONCLUSIONS: Timing of inappropriate organ termination varies across the two sexes in A. palmeri. Our study suggests that the evolution of A. palmeri from a cosexual ancestral state to complete dioecy is still in progress since males exhibited transient hermaphroditism and females produced strictly pistillate flowers.

First evidence of multiple paternity in the blue shark (Prionace glauca).

Multiple paternity (MP) is defined as the behaviour in which females successfully mate with multiple males leading to offspring from different sires within the same litter. MP seems to be frequent and an evolutionary advantage in elasmobranchs. Here the authors report for the first time the occurrence of MP in the cosmopolitan blue shark Prionace glauca L. The evidence, gathered via microsatellite genotyping of pregnant females and their embryos, suggests that MP is very frequent in this species. Knowledge of MP in P. glauca should help describe more precisely its reproductive biology and contribute to the management of its populations.

Evolutionary interactions between thermal ecology and sexual selection.

Thermal ecology and mate competition are both pervasive features of ecological adaptation. A surge of recent work has uncovered the diversity of ways in which temperature affects mating interactions and sexual selection. However, the potential for thermal biology and reproductive ecology to evolve together as organisms adapt to their thermal environment has been underappreciated. Here, we develop a series of hypotheses regarding (1) not only how thermal ecology affects mating system dynamics, but also how mating dynamics can generate selection on thermal traits; and (2) how the thermal consequences of mate competition favour the reciprocal co-adaptation of thermal biology and sexual traits. We discuss our hypotheses in the context of both pre-copulatory and post-copulatory processes. We also call for future work integrating experimental and phylogenetic comparative approaches to understand evolutionary feedbacks between thermal ecology and sexual selection. Overall, studying reciprocal feedbacks between thermal ecology and sexual selection may be necessary to understand how organisms have adapted to the environments of the past and could persist in the environments of the future.

Migration through a Major Andean Ecogeographic Disruption as a Driver of Genetic and Phenotypic Diversity in a Wild Tomato Species.

Evolutionary dynamics at the population level play a central role in creating the diversity of life on our planet. In this study, we sought to understand the origins of such population-level variation in mating systems and defensive acylsugar chemistry in Solanum habrochaites-a wild tomato species found in diverse Andean habitats in Ecuador and Peru. Using Restriction-site-Associated-DNA-Sequencing (RAD-seq) of 50 S. habrochaites accessions, we identified eight population clusters generated via isolation and hybridization dynamics of 4-6 ancestral populations. Detailed characterization of mating systems of these clusters revealed emergence of multiple self-compatible (SC) groups from progenitor self-incompatible populations in the northern part of the species range. Emergence of these SC groups was also associated with fixation of deleterious alleles inactivating acylsugar acetylation. The Amotape-Huancabamba Zone-a geographical landmark in the Andes with high endemism and isolated microhabitats-was identified as a major driver of differentiation in the northern species range, whereas large geographical distances contributed to population structure and evolution of a novel SC group in the central and southern parts of the range, where the species was also inferred to have originated. Findings presented here highlight the role of the diverse ecogeography of Peru and Ecuador in generating population differentiation, and enhance our understanding of the microevolutionary processes that create biological diversity.

What does the distribution of fitness effects of new mutations reflect? Insights from plants.

The distribution of fitness effects (DFE) of new mutations plays a central role in molecular evolution. It is therefore crucial to be able to estimate it accurately from genomic data and to understand the factors that shape it. After a rapid overview of available methods to characterize the fitness effects of mutations, we review what is known on the factors affecting them in plants. Available data indicate that life history traits (e.g. mating system and longevity) have a major effect on the DFE. By contrast, the impact of demography within species appears to be more limited. These results remain to be confirmed, and methods to estimate the joint evolution of demography, life history traits, and the DFE need to be developed.

Global analysis of floral longevity reveals latitudinal gradients and biotic and abiotic correlates.

The length of time a flower remains open and functional - floral longevity - governs important reproductive processes influencing pollination and mating and varies considerably among angiosperm species. However, little is known about large-scale biogeographic patterns and the correlates of floral longevity. Using published data on floral longevity from 818 angiosperm species in 134 families and 472 locations world-wide, we present the first global quantification of the latitudinal pattern of floral longevity and the relationships between floral longevity and a range of biotic and abiotic factors. Floral longevity exhibited a significant phylogenetic signal and was longer at higher latitudes in both northern and southern hemispheres, even after accounting for elevation. This latitudinal variation was associated with several biotic and abiotic variables. The mean temperature of the flowering season had the highest predictive power for floral longevity, followed by pollen number per flower. Surprisingly, compatibility status, flower size, pollination mode, and growth form had no significant effects on flower longevity. Our results suggest that physiological processes associated with floral maintenance play a key role in explaining latitudinal variation in floral longevity across global ecosystems, with potential implications for floral longevity under global climate change and species distributions.

Genomic insights into inter- and intraspecific mating system shifts in Primulina.

The mating system shift from outcrossing to selfing is one of the most frequent evolutionary trends in flowering plants. However, the genomic consequences of this shift remain poorly understood. Specifically, the relative importance of the demographic and genetic processes causing changes in genetic variation and selection efficacy associated with the evolution of selfing is unclear. Here we sequenced the genomes of two Primulina species with contrasting mating systems: P. eburnea (outcrossing) versus P. tabacum (outcrossing, mixed-mating and selfing populations). Whole-genome resequencing data were used to investigate the genomic consequences of mating system shifts within and between species. We found that highly selfing populations of P. tabacum display loss of genetic diversity, increased deleterious mutations, higher genomic burden and fewer adaptive substitutions. However, compared with outcrossing populations, mixed-mating populations did not display loss of genetic diversity and accumulation of genetic load. We find no evidence of population bottlenecks associated with the shift to selfing, which suggests that the genetic effects of selfing on Ne and possibly linked selection, rather than demographic history, are the primary drivers of diversity reduction in highly selfing populations. Our results highlight the importance of distinguishing the relative contribution of mating system and demography on the genomic consequences associated with mating system evolution in plants.

Phylogenomics reveals extensive introgression and a case of mito-nuclear discordance in the killifish genus Kryptolebias.

Introgression is a widespread evolutionary process leading to phylogenetic inconsistencies among distinct parts of the genomes, particularly between mitochondrial and nuclear-based phylogenetic reconstructions (e.g., mito-nuclear discordances). Here, we used mtDNA and genome-wide nuclear sites to provide the first phylogenomic-based hypothesis on the evolutionary relationships within the killifish genus Kryptolebias. In addition, we tested for evidence of past introgression in the genus given the multiple reports of undergoing hybridization between its members. Our mtDNA phylogeny generally agreed with the relationships previously proposed for the genus. However, our reconstruction based on nuclear DNA revealed an unknown lineage - Kryptolebias sp. 'ESP' - as the sister group of the self-fertilizing mangrove killifishes, K. marmoratus and K. hermaphroditus. All individuals sequenced of Kryptolebias sp. 'ESP' had the same mtDNA haplotype commonly observed in K. hermaphroditus, demonstrating a clear case of mito-nuclear discordance. Our analysis further confirmed extensive history of introgression between Kryptolebias sp. 'ESP' and K. hermaphroditus. Population genomics analyses indicate no current gene flow between the two lineages, despite their current sympatry and history of introgression. We also confirmed introgression between other species pairs in the genus that have been recently reported to form hybrid zones. Overall, our study provides a phylogenomic reconstruction covering most of the Kryptolebias species, reveals a new lineage hidden in a case of mito-nuclear discordance, and provides evidence of multiple events of ancestral introgression in the genus. These findings underscore the importance of investigating different genomic information in a phylogenetic framework, particularly in taxa where introgression is common as in the sexually diverse mangrove killifishes.

A tangled web: Comparing inter- and intraspecific mating dynamics in Anasa squash bugs.

Reproductive interference, reproductive interactions between heterospecific individuals including mating, is commonly reported across taxa, but its drivers are still unclear. Studying interspecific matings in the context of their conspecific mating system-by relating an individual's conspecific mating behaviour to its heterospecific interactions-offers a powerful approach to address this uncertainty. Here, we compare inter- and intraspecific mating dynamics in the squash bug Anasa tristis and its close relative Anasa andresii under semi-natural conditions. Using replicated enclosures, we surveyed the mating behaviour of individually marked A. tristis and A. andresii (five males and five females of each species per trial) at hourly intervals using a robotic camera system over a 14-day period. We uncovered high levels of reproductive interference (19% of individuals engaged in interspecific matings), but the majority of mating activity took place between conspecifics. A. tristis females which engaged in interspecific matings had comparable hatching success with those which did not. Therefore, in this system, relatively high levels of reproductive interference may emerge under semi-natural conditions as a by-product of limited intraspecific pre-copulatory choice paired with limited fitness penalties for at least one of the species involved.

Floral orientation affects outcross-pollen deposition in buzz-pollinated flowers with bilateral symmetry.

PREMISE: Floral orientation is central to plant-pollinator interactions and is commonly associated with floral symmetry. Bilaterally symmetrical flowers are often oriented horizontally for optimal pollinator positioning and pollen transfer efficiency, while the orientation of radially symmetrical flowers is variable. Buzz-pollinated species (pollinated by vibration-producing bees) include bilateral, horizontally oriented flowers, and radial, pendant flowers. The effect of floral orientation on pollen transfer has never been tested in buzz-pollinated species. METHODS: Here, we examined the effect of floral orientation on bumblebee-mediated pollen deposition in three buzz-pollinated Solanum species with different floral symmetry and natural orientations: S. lycopersicum and S. seaforthianum (radial, pendant), and S. rostratum (bilateral, horizontal). We tested whether orientation affects total stigmatic pollen deposition (both self and outcross pollen) when all flowers have the same orientation (either pendant or horizontal). In a second experiment, we evaluated whether different orientations of donor and recipient flowers affects the receipt of outcross pollen by S. rostratum. RESULTS: For the three Solanum species studied, there was no effect of floral orientation on total pollen deposition (both self and outcross) when flowers shared the same orientation. In contrast, in our experiment with S. rostratum, we found that pendant flowers received fewer outcross-pollen grains when paired with pendant donors. CONCLUSIONS: We suggest that floral orientation influences the quality of pollen transferred, with more outcross pollen transferred to horizontally oriented recipients in the bilaterally symmetrical S. rostratum. Whether other bilaterally symmetrical, buzz-pollinated flowers also benefit from increased cross-pollination when presented horizontally remains to be established.

Conserved transcriptomic profiles underpin monogamy across vertebrates.

Social monogamy, typically characterized by the formation of a pair bond, increased territorial defense, and often biparental care, has independently evolved multiple times in animals. Despite the independent evolutionary origins of monogamous mating systems, several homologous brain regions and neuropeptides and their receptors have been shown to play a conserved role in regulating social affiliation and parental care, but little is known about the neuromolecular mechanisms underlying monogamy on a genomic scale. Here, we compare neural transcriptomes of reproductive males in monogamous and nonmonogamous species pairs of Peromyscus mice, Microtus voles, parid songbirds, dendrobatid frogs, and Xenotilapia species of cichlid fishes. We find that, while evolutionary divergence time between species or clades did not explain gene expression similarity, characteristics of the mating system correlated with neural gene expression patterns, and neural gene expression varied concordantly across vertebrates when species transition to monogamy. Our study provides evidence of a universal transcriptomic mechanism underlying the evolution of monogamy in vertebrates.

Mating Systems and Seed Reproduction in Gynodioecious Geranium asiaticum (Geraniaceae).

Mating systems and seed reproduction in gynodioecious Geranium asiaticum Serg. (G. bifolium Patrin.) were studied in four coenopopulations of Western Siberia (Novosibirsk region). The bisexual flower of hermaphrodite individuals of G. asiaticum is characterized by a longer flowering (2.5-3.5 days) than the pistillate flower of female individuals (2-2.5 days), due to the passage of the male (staminate) phase at the beginning of morphogenesis: G. asiaticum is characterized by strict protandry. Mating of individuals of G. asiaticum occurs according to the type of xenogamy, autogamy is completely excluded. In an experiment to isolate individual flowers, 100% of isolated pistillate and bisexual flowers dried up without fertilization. In an experiment on artificial pollination of flowers, 85% (17 out of 20 flowers) of pistillate flowers formed fruits, whereas only 10% (3 out of 30 flowers) of bisexual flowers formed fruits. There were no significant differences in the number of flowers on the generative shoot in female and hermaphrodite individuals. Significant differences were found between heterosexual individuals in terms of the number of fruits and the number of seeds per generative shoot: female individuals formed 16.1-22.1 times more fruits and 13.8-28.3 times more seeds than hermaphrodites. Pistillate flowers formed an average of 1.85 ± 0.08 seeds per flower, and bisexual flowers 0.07 ± 0.02 seeds per flower, i.e., on average, female plants form 26.4 times more seeds than hermaphrodites. It was found that the fruits and seeds were formed mainly by female individuals, but hermaphrodite individuals produced the pollen necessary for fertilization. The different degree of sexual differentiation of G. asiaticum and Geranium sylvaticum L. suggests that in genus Geranium there are transformations in direction of the formation of dioecy.

Diversification or Collapse of Self-Incompatibility Haplotypes as a Rescue Process.

AbstractIn angiosperm self-incompatibility systems, pollen with an allele matching the pollen recipient at the self-incompatibility locus is rejected. Extreme allelic polymorphism is maintained by frequency-dependent selection favoring rare alleles. However, two challenges result in a chicken-or-egg problem for the spread of a new allele (a tightly linked haplotype in this case) under the widespread "collaborative non-self-recognition" mechanism. A novel pollen function mutation alone would merely grant compatibility with a nonexistent style function allele: a neutral change at best. A novel pistil function mutation alone could be fertilized only by pollen with a nonexistent pollen function allele: a deleterious change that would reduce seed set to zero. However, a pistil function mutation complementary to a previously neutral pollen mutation may spread if it restores self-incompatibility to a self-compatible intermediate. We show that novel haplotypes can also drive elimination of existing ones with fewer siring opportunities. We calculate relative probabilities of increase and collapse in haplotype number given the initial collection of incompatibility haplotypes and the population gene conversion rate. Expansion in haplotype number is possible when population gene conversion rate is large, but large contractions are likely otherwise. A Markov chain model derived from these expansion and collapse probabilities generates a stable haplotype number distribution in the realistic range of 10-40 under plausible parameters. However, smaller populations might lose many haplotypes beyond those lost by chance during bottlenecks.

Evolution of seed mass associated with mating systems in multiple plant families.

In flowering plants, the evolution of self-fertilization (selfing) from obligate outcrossing is regarded as one of the most prevalent evolutionary transitions. The evolution of selfing is often accompanied by various changes in genomic, physiological and morphological properties. In particular, a set of reproductive traits observed typically in selfing species is called the "selfing syndrome". A mathematical model based on the kinship theory of genetic imprinting predicted that seed mass should become smaller in selfing species compared with outcrossing congeners, as a consequence of the reduced conflict between maternally and paternally derived alleles in selfing plants. Here, we test this prediction by examining the association between mating system and seed mass across a wide range of taxa (642 species), considering potential confounding factors: phylogenetic relationships and growth form. We focused on three plant families-Solanaceae, Brassicaceae and Asteraceae-where information on mating systems is abundant, and the analysis was performed for each family separately. When phylogenetic relationships were controlled, we consistently observed that selfers (represented by self-compatible species) tended to have a smaller seed mass compared with outcrossers (represented by self-incompatible species) in these families. In summary, our analysis suggests that small seeds should also be considered a hallmark of the selfing syndrome, although we note that mating systems have relatively small effects on seed mass variation.

Isolation and characterization of microsatellites markers in Centaurium grandiflorum ssp. boissieri.

BACKGROUND: Estimating outcrossing/selfing rates and characterizing genetic diversity with microsatellite markers are crucial to understanding the evolution of plant mating systems. METHODS AND RESULTS: We developed, optimized and characterized eight new primer pairs for Centaurium grandiflorum ssp. boissieri and transferred them to three subspecies of Centaurium quadrifolium. Two SSR loci were transferred from Sabatia campestris to the four Centaurium taxa. Polymorphisms, He, Ho and H-W deviations were estimated in two populations of C. grandiflorum ssp. boissieri and in seven individuals each of C. quadrifolium ssp. barrelieri, C. quadrifolium ssp. parviflorum and C. quadrifolium ssp. quadrifolium. A total of 80 individuals was used in these experiments. The number of polymorphic loci varied among species from one to ten. A total of 127 alleles was scored. The average number of alleles per locus was 12.7. He was higher than Ho in all sampled populations. Hardy-Weinberg equilibrium was found for some loci in different species. CONCLUSIONS: This is the first report of microsatellites successfully amplified in the whole Centaurium genus. They will be valuable for estimating mating system parameters and genetic diversity and exploring their relationships with the wide variation in flower morphology in the genus, especially anther-stigma separation.

Inbreeding depresses altruism in a cooperative society.

In some animal species, individuals regularly breed with relatives, including siblings and parents. Given the high fitness costs of inbreeding, evolutionary biologists have found it challenging to understand the persistence of these inbred societies in nature. One appealing but untested explanation is that early life care may create a benign environment that offsets inbreeding depression, allowing inbred societies to evolve. We test this possibility using 21 years of data from a wild cooperatively breeding mammal, the banded mongoose, a species where almost one in ten young result from close inbreeding. We show that care provided by parents and alloparents mitigates inbreeding depression for early survival. However, as adults, inbred individuals provide less care, reducing the amount of help available to the next generation. Our results suggest that inbred cooperative societies are rare in nature partly because the protective care that enables elevated levels of inbreeding can be reduced by inbreeding depression.