Imitating the cost of males: A hypothesis for coexistence of all‐female sperm‐dependent species and their sexual host

All‐female sperm‐dependent species are particular asexual organisms that must coexist with a closely related sexual host for reproduction. However, demographic advantages of asexual over sexual species that have to produce male individuals could lead both to extinction. The unresolved question of their coexistence still challenges and fascinates evolutionary biologists. As an alternative hypothesis, we propose those asexual organisms are afflicted by a demographic cost analogous to the production of males to prevent exclusion of the host. Previously proposed hypotheses stated that asexual individuals relied on a lower fecundity than sexual females to cope with demographic advantage. In contrast, we propose that both sexual and asexual species display the same number of offspring, but half of asexual individuals imitate the cost of sex by occupying ecological niches but producing no offspring. Simulations of population growth in closed systems under different demographic scenarios revealed that only the presence of nonreproductive individuals in asexual females can result in long‐term coexistence. This hypothesis is supported by the fact that half of the females in some sperm‐dependent organisms did not reproduce clonally.     

Male mate choice and sperm allocation in a sexual/asexual mating complex of Poecilia (Poeciliidae, Teleostei)

Male mate choice is critical for understanding the evolution and maintenance of sexual/asexual mating complexes involving sperm-dependent, gynogenetic species. Amazon mollies (Poecilia formosa) require sperm to trigger embryogenesis, but the males (e.g. Poecilia mexicana) do not contribute genes. Males benefit from mating with Amazon mollies, because such matings make males more attractive to conspecific females, but they might control the cost of such matings by providing less sperm to Amazon mollies. We examined this at the behavioural and sperm levels. P. mexicana males preferred to mate with, and transferred more sperm to conspecific females. However, if males mated with P. formosa, sperm was readily transferred. This underscores the importance of male choice in this system.     

Rapid local adaptation in both sexual and asexual invasive populations of monkeyflowers (Mimulus spp.)

Background and AimsTraditionally, local adaptation has been seen as the outcome of a long evolutionary history, particularly with regard to sexual lineages. By contrast, phenotypic plasticity has been thought to be most important during the initial stages of population establishment and in asexual species. We evaluated the roles of adaptive evolution and phenotypic plasticity in the invasive success of two closely related species of invasive monkeyflowers (Mimulus) in the UK that have contrasting reproductive strategies: M. guttatus combines sexual (seeds) and asexual (clonal growth) reproduction while M. × robertsii is entirely asexual.MethodsWe compared the clonality (number of stolons), floral and vegetative phenotype, and phenotypic plasticity of native (M. guttatus) and invasive (M. guttatus and M. × robertsii) populations grown in controlled environment chambers under the environmental conditions at each latitudinal extreme of the UK. The goal was to discern the roles of temperature and photoperiod on the expression of phenotypic traits. Next, we tested the existence of local adaptation in the two species within the invasive range with a reciprocal transplant experiment at two field sites in the latitudinal extremes of the UK, and analysed which phenotypic traits underlie potential local fitness advantages in each species.Key ResultsPopulations of M. guttatus in the UK showed local adaptation through sexual function (fruit production), while M. × robertsii showed local adaptation via asexual function (stolon production). Phenotypic selection analyses revealed that different traits are associated with fitness in each species. Invasive and native populations of M. guttatus had similar phenotypic plasticity and clonality. M. × robertsii presents greater plasticity and clonality than native M. guttatus, but most populations have restricted clonality under the warm conditions of the south of the UK.ConclusionsThis study provides experimental evidence of local adaptation in a strictly asexual invasive species with high clonality and phenotypic plasticity. This indicates that even asexual taxa can rapidly (<200 years) adapt to novel environmental conditions in which alternative strategies may not ensure the persistence of populations.     

Compartmentalization and niche differentiation: causal patterns of competition and coexistence

The current major models of coexistence of species on the same resources are briefly summarized. It is then shown that analysis of supposedly competitive systems in terms of the physical four dimensions of phase-space is sufficient to understand the causes for coexistence and for competitive exclusion. Thus, the multiple dimensions of niche theory are reduced to factors which define the magnitudes of the phase-spatial system, in particular the boundaries of population spaces and of periods of activity. Excluding possible cooperative interaction between consumers, it appears that coexistence of species on thesame kind of limiting resource is possible only in cases of compartmentalization either in space, or in time, of resource consumption, i.e. if each consumer species disposes of a separate resource supply. Three criteria were found to be decisive for successful compartmentalization (i.e. for coexistence): 1. the vector of the resource flow; 2. relative mobility between consumers and resource units; 3. dependence or independence of resource flow on previous consumption. The traditional terminology of niche theory and of competition theory in general proved to be inadequate for analytical treatment of problems of coexistence.     

Liking the good guys: amplifying local adaptation via the evolution of condition‐dependent mate choice

Local adaptation can be strengthened through a diversity of mechanisms that reduce gene flow between contrasting environments. Recent work revealed that mate choice could enhance local adaptation when females preferentially mate with locally adapted males and that such female preferences readily evolve, but the opposing effects of recombination, migration and costs of female preferences remain relatively unexplored. To investigate these effects, we develop a two‐patch model with two genes, one influencing an ecological trait and one influencing female preferences, where both male signals and female preferences are allowed to depend on the match between an individual's ecological trait and the local environment (condition). Because trait variation is limited when migration is rare and the benefits of preferential mating are short‐lived when migration is frequent, we find that female preferences for males in high condition spread most rapidly with intermediate levels of migration. Surprisingly, we find that preferences for locally adapted males spread fastest with higher recombination rates, which contrasts with earlier studies. This is because a stronger preference allele for locally adapted males can only get uncoupled from maladapted ecological alleles following migration through recombination. The effects of migration and recombination depend strongly on the condition of the males being chosen by females, but only weakly on the condition of the females doing the choosing, except when it comes to the costs of preference. Although costs always impede the spread of female preferences for locally adapted males, the impact is substantially lessened if costs are borne primarily by females in poor condition. The abundance of empirical examples of condition‐dependent mate choice combined with our theoretical results suggests that the evolution of mate choice could commonly facilitate local adaptation in nature.     

Micro-habitat niche differentiation contributing to coexistence of Eucryptorrhynchus scrobiculatus Motschulsky and Eucryptorrhynchus brandti (Harold)*

Temporal, spatial, and trophic niche differentiation usually occurs among species living in similar habitats which can reduce interspecific competition under limited resources. Eucryptorrhynchus scrobiculatus and Eucryptorrhynchus brandti are sympatric and closely related species and are host-specific to Ailanthus altissima (Mill.) Swingle in China. However, the possibility of niche differentiation between the two species is not clear. Therefore, we investigated the density of the two weevils temporally, spatially, and trophically (plant parts of A. altissima) at Lingwu farm and Haojiaqiao town, Lingwu city, Ningxia Hui Autonomous Region. No differences were found in temporal Levin’s niche breath index values ranging from 3.74 to 3.95 and temporal Pianka’s niche overlap values (0.98–0.99). There was little differentiation in the vertical spatial niche. The vertical distribution of E. scrobiculatus was mainly located from 0?cm (ground) to over 250?cm on tree-of-heaven. Eucryptorrhynchus brandti was found predominantly from 0.1 to 50?cm to over 250?cm on tree-of-heaven. The overlap of the cardinal direction spatial niche was 0.90–0.98, indicating no significant overlap in the cardinal direction at Lingwu farm and Haojiaqiao town. Significant differentiation of trophic niche occurred with E. scrobiculatus feeding on 1-year-old branches, perennial branches, and petioles, while E. brandti feed on the stem.     

Off to new shores: Climate niche expansion in invasive mosquitofish (Gambusia spp.)

AimFormerly introduced for their presumed value in controlling mosquito‐borne diseases, the two mosquitofish Gambusia affinis and G. holbrooki (Poeciliidae) are now among the world''s most widespread invasive alien species, negatively impacting aquatic ecosystems around the world. These inconspicuous freshwater fish are, once their presence is noticed, difficult to eradicate. It is, therefore, of utmost importance to assess their geographic potential and to identify their likely ability to persist under novel climatic conditions.LocationGlobal.MethodsWe build species distribution models using occurrence data from the native and introduced distribution ranges to identify putative niche shifts and further ascertain the areas climatically suitable for the establishment and possible spread of mosquitofish.ResultsWe found significant niche expansions into climatic regions outside their natural climatic conditions, emphasizing the importance of integrating climatic niches of both native and invasive ranges into projections. In particular, there was a marked shift toward tropical regions in Asia and a clear niche shift of European G. holbrooki. This ecological flexibility partly explains the massive success of the two species, and substantially increases the risk for further range expansion. We also showed that the potential for additional expansion resulting from climate change is enormous—especially in Europe.Main conclusionsDespite the successful invasion history and ongoing range expansions, many countries still lack proper preventive measures. Thus, we urge policy makers to carefully evaluate the risk both mosquitofish pose to a particular area and to initiate appropriate management strategies.     

How to go extinct by mating too much: population consequences of male mate choice and efficiency in a sexual–asexual species complex

Selection acting on individuals is not predicted to maximize population persistence, yet examples that explicitly quantify conflicts between individual and population level benefits are scarce. One such conflict occurs over sexual reproduction because of the cost of sex: sexual populations that suffer the cost of producing males have only half the growth rate compared to asexuals. Male behaviour can additionally impact population dynamics in a variety of ways, and here we study an example where the impact is unusually clear: the riddle of persistence of sperm‐dependent sexual–asexual species complexes. Here, a sexually reproducing host species coexists with an ameiotically reproducing all‐female sperm parasite. Sexual–asexual coexistence should not be stable because the proportion of asexually reproducing females will rapidly increase and the relative abundance of the sexually reproducing host species will decline. A severe shortage of males will lead to sperm limitation for sexual and asexual females and the system collapses. Male mate choice could reduce the reproductive potential of the asexual species and thus potentially prevent the collapse. In the gynogenetic (sperm‐dependent parthenogenetic) Amazon molly Poecilia formosa and its host (P. latipinna or P. mexicana), males discriminate against asexual females to some extent. Using a population‐dynamical model, we examine the population dynamics of this species complex with varying strengths of male discrimination ability and efficiency with which they locate females and produce sperm. The sexual species would benefit from stronger discrimination, thus preventing being displaced by the asexual females. However, males would be required to evolve preferences that are probably too strong to be purely based upon selection acting on individuals. We conclude that male behaviour does not fully prevent but delays extinction, yet this is highly relevant because low local extinction rates strongly promote coexistence as a metapopulation.     

Breeding behavior of female white‐tailed deer relative to conception: Evidence for female mate choice

Female white‐tailed deer (Odocoileus virginianus) are thought to choose between two behavioral strategies to maximize the quality of potential mates: sit and wait, characterized by concentrating activity within a restricted area, and excursive behavior, characterized by increased activity and excursions outside the home range. As movement patterns may influence conception, our goal was to examine the patterns of female white‐tailed deer movements to evaluate which breeding strategy was employed. We equipped 36 female white‐tailed deer with GPS collars from August 2013 to December 2015. We found that movement rate and probability of activity were greatest near the peak of the breeding season, and we observed increases in both metrics during the 40 days prior to estimated conception. Peak size of home range and core area occurred in the days surrounding conception. We found that 11 deer performed an excursion, ranging from 43 days before until 36 days after conception, with the peak probability of being outside of an individual home range occurring 1 day prior to conception. Our results suggest that female white‐tailed deer may attempt to maximize the quality of their mates by advertising availability for breeding through excursive behaviors just prior to entering estrus.     

Figs (Ficus spp.) and fig wasps (Chalcidoidea, Agaonidae): hypotheses for an ancient symbiosis

Figs and their pollinating fig wasps are dependent on one another for propagation of their own kinds. The wasps reproduce by ovipositing through the styles of female flowers within the closed fig receptacles (syconia). About half of the female flowers within the syconia of monoecious figs have styles which are longer than the ovipositors of the wasp, and they will therefore produce seeds rather than wasp larvae. Since a longer ovipositor would enable a wasp to reach more ovules and deposit more eggs, the question arises at to why longer ovipositors have not evolved.
In an attempt to answer this question, four seemingly plausible hypotheses are examined but each is shown to be problematical in some way. Consideration is then given to a fifth hypothesis which proposes that ovipositor length is constrained by abortion of syconia with relatively few seed embryos and many agaonid larvae. It is argued first that this pattern of abortion will be selected during a sustained period of heavy wasp infestation because seeds will then become scarce relative to pollen-carrying wasps. Increased expenditure by the fig on seed production would therefore be favoured by natural selection. A greater expenditure on seeds would occur if young syconia with exceptionally heavy wasp infestations were dropped and the saved nutrients invested in syconia of a subsequent crop containing average levels of wasp larvae and seeds. Provided that the energy and nutrient cost of dropping young syconia is small, the selective advantage to the wasp of longer ovipositors is eliminated in this way. A stable coexistence of figs and wasps is therefore possible. The paper concludes by discussing two general predictions of the abortion hypothesis, and how these may be tested.     

The relationship of male-male mounting to mate choice and sexual performance in male dairy goats

Rearing of male farm animals in unisexual groups has been implicated as a factor contributing to the failure of many males to breed as adults. The present study examines the relationship of male-male mounting in yearling dairy goats to subsequent mate preferences and sexual performance.Twenty-four sexually inexperienced male dairy goats, representing the Alpine, LaMancha, Saanen and Toggenburg breeds, were observed for male-male mounting in their home enclosure and then tested for mate choice and sexual performance when exposed to male and female (estrous and diestrous) stimulus animals. Their sexual behavior was compared with 7 adult goats with previous breeding experience.In the mate choice-sexual performance tests, 4 sexually inexperienced goats (17%) were sexually inactive, 6 (25%) mounted both male and female stimulus animals and 14 (58%) mounted only the female stimuli. Mate choice and sexual performance of the 20 sexually active males was not related to the number of male-male mounts initiated or the number of different males mounted in their home enclosure. However, the goats that received the greatest number of mounts in their home pen tended to be bisexual (would mount both male and female stimulus animals) in the mate choice tests. Males that were sexually inactive in mate choice-sexual performance tests repeatedly mounted the same male during home pen observations. Except for ejaculation frequency, the sexual performance of the sexually naive and experienced goats was similar. Goats of the Saanen breed were favored recipients of mounts from other males. There was no relationship between the number of male-male mounts performed and received.It was hypothesized that the reproductive failure of many male farm animals reared in all-male groups may be more closely related to the formation of specific sexual attachments to other males rather than the frequency with which they exhibit homosexual behaviors.     

The Plasmodium falciparum, Nima-related kinase Pfnek-4: a marker for asexual parasites committed to sexual differentiation

ABSTRACT: BACKGROUND: Malaria parasites undergo, in the vertebrate host, a developmental switch from asexual replication to sexual differentiation leading to the formation of gametocytes, the only form able to survive in the mosquito vector. Regulation of the onset of the sexual phase remains largely unknown and represents an important gap in the understanding of the parasite's complex biology. METHODS: The expression and function of the Nima-related kinase Pfnek-4 during the early sexual development of the human malaria parasite Plasmodium falciparum were investigated, using three types of transgenic Plasmodium falciparum 3D7 lines: (i) episomally expressing a Pfnek-4-GFP fusion protein under the control of its cognate pfnek-4 promoter; (ii) episomally expressing negative or positive selectable markers, yeast cytosine deaminase-uridyl phosphoribosyl transferase, or human dihydrofolate reductase, under the control of the pfnek-4 promoter; and (iii) lacking a functional pfnek-4 gene. Parasite transfectants were analysed by fluorescence microscopy and flow cytometry. In vitro growth rate and gametocyte formation were determined by Giemsa-stained blood smears. RESULTS: The Pfnek-4-GFP protein was found to be expressed in stage II to V gametocytes and, unexpectedly, in a subset of asexual-stage parasites undergoing schizogony. Culture conditions stimulating gametocyte formation resulted in significant increase of this schizont subpopulation. Moreover, sorted asexual parasites expressing the Pfnek-4-GFP protein displayed elevated gametocyte formation when returned to in vitro culture in presence of fresh red blood cells, when compared to GFP- parasites from the same initial population. Negative selection of asexual parasites expressing pfnek-4 showed a marginal reduction in growth rate, whereas positive selection caused a marked reduction in parasitaemia, but was not sufficient to completely abolish proliferation. Pfnek-4- clones are not affected in their asexual growth and produced normal numbers of stage V gametocytes. CONCLUSIONS: The results indicate that Pfnek-4 is not strictly gametocyte-specific, and is expressed in a small subset of asexual parasites displaying high rate conversion to sexual development. Pfnek-4 is not required for erythrocytic schizogony and gametocytogenesis. This is the first study to report the use of a molecular marker for the sorting of sexually-committed schizont stage P. falciparum parasites, which opens the way to molecular characterization of this pre-differentiated subpopulation.     

Patterns of MHC‐dependent mate selection in humans and nonhuman primates: a meta‐analysis

Genes of the major histocompatibility complex (MHC) in vertebrates are integral for effective adaptive immune response and are associated with sexual selection. Evidence from a range of vertebrates supports MHC‐based preference for diverse and dissimilar mating partners, but evidence from human mate choice studies has been disparate and controversial. Methodologies and sampling peculiarities specific to human studies make it difficult to know whether wide discrepancies in results among human populations are real or artefact. To better understand what processes may affect MHC‐mediated mate choice across humans and nonhuman primates, we performed phylogenetically controlled meta‐analyses using 58 effect sizes from 30 studies across seven primate species. Primates showed a general trend favouring more MHC‐diverse mates, which was statistically significant for humans. In contrast, there was no tendency for MHC‐dissimilar mate choice, and for humans, we observed effect sizes indicating selection of both MHC‐dissimilar and MHC‐similar mates. Focusing on MHC‐similar effect sizes only, we found evidence that preference for MHC similarity was an artefact of population ethnic heterogeneity in observational studies but not among experimental studies with more control over sociocultural biases. This suggests that human assortative mating biases may be responsible for some patterns of MHC‐based mate choice. Additionally, the overall effect sizes of primate MHC‐based mating preferences are relatively weak (Fisher's Z correlation coefficient for dissimilarity Zr = 0.044, diversity Zr = 0.153), calling for careful sampling design in future studies. Overall, our results indicate that preference for more MHC‐diverse mates is significant for humans and likely conserved across primates.     

The hidden benefits of sex: Evidence for MHC‐associated mate choice in primate societies

Major histocompatibility complex (MHC)‐associated mate choice is thought to give offspring a fitness advantage through disease resistance. Primates offer a unique opportunity to understand MHC‐associated mate choice within our own zoological order, while their social diversity provides an exceptional setting to examine the genetic determinants and consequences of mate choice in animal societies. Although mate choice is constrained by social context, increasing evidence shows that MHC‐dependent mate choice occurs across the order in a variety of socio‐sexual systems and favours mates with dissimilar, diverse or specific genotypes non‐exclusively. Recent research has also identified phenotypic indicators of MHC quality. Moreover, novel findings rehabilitate the importance of olfactory cues in signalling MHC genes and influencing primate mating decisions. These findings underline the importance to females of selecting a sexual partner of high genetic quality, as well as the generality of the role of MHC genes in sexual selection.     

(Patho‐)physiological relevance of PINK1‐dependent ubiquitin phosphorylation

Mutations in PINK1 and PARKIN cause recessive, early‐onset Parkinson's disease (PD). Together, these two proteins orchestrate a protective mitophagic response that ensures the safe disposal of damaged mitochondria. The kinase PINK1 phosphorylates ubiquitin (Ub) at the conserved residue S65, in addition to modifying the E3 ubiquitin ligase Parkin. The structural and functional consequences of Ub phosphorylation (pS65‐Ub) have already been suggested from in vitro experiments, but its (patho‐)physiological significance remains unknown. We have generated novel antibodies and assessed pS65‐Ub signals in vitro and in cells, including primary neurons, under endogenous conditions. pS65‐Ub is dependent on PINK1 kinase activity as confirmed in patient fibroblasts and postmortem brain samples harboring pathogenic mutations. We show that pS65‐Ub is reversible and barely detectable under basal conditions, but rapidly induced upon mitochondrial stress in cells and amplified in the presence of functional Parkin. pS65‐Ub accumulates in human brain during aging and disease in the form of cytoplasmic granules that partially overlap with mitochondrial, lysosomal, and total Ub markers. Additional studies are now warranted to further elucidate pS65‐Ub functions and fully explore its potential for biomarker or therapeutic development.     

Forest responses to simulated elevated CO2 under alternate hypotheses of size‐ and age‐dependent mortality

Elevated atmospheric carbon dioxide (eCO₂) is predicted to increase growth rates of forest trees. The extent to which increased growth translates to changes in biomass is dependent on the turnover time of the carbon, and thus tree mortality rates. Size‐ or age‐dependent mortality combined with increased growth rates could result in either decreased carbon turnover from a speeding up of tree life cycles, or increased biomass from trees reaching larger sizes, respectively. However, most vegetation models currently lack any representation of size‐ or age‐dependent mortality and the effect of eCO₂ on changes in biomass and carbon turnover times is thus a major source of uncertainty in predictions of future vegetation dynamics. Using a reduced‐complexity form of the vegetation demographic model the Functionally Assembled Terrestrial Ecosystem Simulator to simulate an idealised tropical forest, we find increases in biomass despite reductions in carbon turnover time in both size‐ and age‐dependent mortality scenarios in response to a hypothetical eCO₂‐driven 25% increase in woody net primary productivity (wNPP). Carbon turnover times decreased by 9.6% in size‐dependent mortality scenarios due to a speeding up of tree life cycles, but also by 2.0% when mortality was age‐dependent, as larger crowns led to increased light competition. Increases in aboveground biomass (AGB) were much larger when mortality was age‐dependent (24.3%) compared with size‐dependent (13.4%) as trees reached larger sizes before death. In simulations with a constant background mortality rate, carbon turnover time decreased by 2.1% and AGB increased by 24.0%, however, absolute values of AGB and carbon turnover were higher than in either size‐ or age‐dependent mortality scenario. The extent to which AGB increases and carbon turnover decreases will thus depend on the mechanisms of large tree mortality: if increased size itself results in elevated mortality rates, then this could reduce by about half the increase in AGB relative to the increase in wNPP.     

Female‐induced remote regulation of sperm physiology may provide opportunities for gamete‐level mate choice

In sedentary externally fertilizing species, direct interactions between mating partners are limited and prefertilization communication between sexes occurs largely at the gamete level. Certain combinations of eggs and sperm often have higher fertilization success than others, which may be contingent on egg‐derived chemical factors that preferentially attract sperm from compatible males. Here, we examine the mechanisms underlying such effects in the marine mussel Mytilus galloprovincialis, where differential sperm attraction has recently been shown to be associated with variation in offspring viability. Specifically, we focus on the sperm surface glycans, an individually unique layer of carbohydrates that moderate self‐recognition and other cellular‐level interactions. In many species egg‐derived factors trigger remarkable changes in the sperm's glycan layer, physiology, and swimming behavior, and thus potentially moderate mate choice at the gamete level. Here, we show that sperm glycan modifications and the strength of acrosome reaction are both dependent on specific male–female interactions (male–female combination). We also find associations between female‐induced sperm glycan changes and the Ca²⁺ influx into sperm–‐a key regulator of fertilization processes from sperm capacitation to gamete fusion. Together, our results suggest that female‐induced remote regulation of sperm physiology may constitute a novel mechanism of gamete‐level mate choice.