Asexual evolution: do intragenomic parasites maintain sex?

Resolving the paradox of sex, with its twofold cost to genic transmission, remains one of the major unresolved questions in evolutionary biology. Counting this genetic cost has now gone genomic. In this issue of Molecular Ecology, Kraaijeveld et al. (2012) describe the first genome‐scale comparative study of related sexual and asexual animal lineages, to test the hypothesis that asexuals bear heavier loads of deleterious transposable elements. A much higher density of such parasites might be expected, due to the inability of asexual lineages to purge transposons via mechanisms exclusive to sexual reproduction. They find that the answer is yes—and no—depending upon the family of transposons considered. Like many such advances in testing theory, more questions are raised by this study than answered, but a door has been opened to molecular evolutionary analyses of how responses to selection from intragenomic parasites might mediate the costs of sex.     

Use of genotyping by sequencing data to develop a high‐throughput and multifunctional SNP panel for conservation applications in Pacific lamprey

Next‐generation sequencing data can be mined for highly informative single nucleotide polymorphisms (SNPs) to develop high‐throughput genomic assays for nonmodel organisms. However, choosing a set of SNPs to address a variety of objectives can be difficult because SNPs are often not equally informative. We developed an optimal combination of 96 high‐throughput SNP assays from a total of 4439 SNPs identified in a previous study of Pacific lamprey (Entosphenus tridentatus) and used them to address four disparate objectives: parentage analysis, species identification and characterization of neutral and adaptive variation. Nine of these SNPs are F_ST outliers, and five of these outliers are localized within genes and significantly associated with geography, run‐timing and dwarf life history. Two of the 96 SNPs were diagnostic for two other lamprey species that were morphologically indistinguishable at early larval stages and were sympatric in the Pacific Northwest. The majority (85) of SNPs in the panel were highly informative for parentage analysis, that is, putatively neutral with high minor allele frequency across the species’ range. Results from three case studies are presented to demonstrate the broad utility of this panel of SNP markers in this species. As Pacific lamprey populations are undergoing rapid decline, these SNPs provide an important resource to address critical uncertainties associated with the conservation and recovery of this imperiled species.     

To be,or not to be,related: how female guppies bias sperm usage

In the Descent of Man, Darwin wrote “the power to charm the female has sometimes been more important than the power to conquer other males in battle” (Darwin 1871 ). Since his pioneering work, the field of sexual selection has exploded as biologists strive to understand how females bias fertilization towards preferred males. In the context of genetic relatedness between potential mates, two main hypotheses exist to explain female mating preferences. First, a female may bias fertilization towards genetically dissimilar males if she gains evolutionary fitness through the production of genetically diverse offspring – a model known as dissortative mating or inbreeding avoidance. Second, a female may favour genetically similar males if her offspring are more likely to inherit coadapted gene complexes – a model known as assortative mating or outbreeding avoidance. In this issue of Molecular Ecology, Gasparini et al. (2015) demonstrate that female guppies bias fertilization towards males which are more related to them at major histocompatibility (MHC) class IIB genes. Amazingly, this bias occurs after insemination of sperm from two different males.     

Puny males punch above their weight to preserve genetic diversity in a declining Atlantic salmon population

Many salmonid fish populations have anadromous (i.e. migratory) and nonanadromous individuals co‐existing in sympatry. The nonanadromous individuals, frequently males, mature at a much smaller size in freshwater without undergoing marine migrations and often successfully fertilize many eggs laid by anadromous females. Because these small males do not recruit to fisheries, they are often not regarded in high esteem by fishers. In this issue of Molecular Ecology, Johnstone et al. ( 2013 ) demonstrate that by substantially contributing to reproduction, such males help maintain genetic diversity in a declining population of Atlantic salmon (Salmo salar). Their results show that estimates of effective population size (N_e), obtained by counting the number of anadromous adults returning from sea and correcting for unequal sex ratios, are lower than estimates generated from genetic markers. Many mechanisms are expected to reduce N_e below the adult census population size (N); the opposite pattern of N_e > N observed by Johnstone et al. ( 2013 ) is difficult to explain unless the reproductive effort of nonanadromous males is accounted for. The results have important implications for the conservation of small populations and highlight the challenges of relating N_e to N in organisms with complex life histories.     

Boechera, a model system for ecological genomics

The selection and development of a study system for evolutionary and ecological functional genomics (EEFG) depend on a variety of factors. Here, we present the genus Boechera as an exemplary system with which to address ecological and evolutionary questions. Our focus on Boechera is based on several characteristics as follows: (i) native populations in undisturbed habitats where current environments reflect historical conditions over several thousand years; (ii) functional genomics benefitting from its close relationship to Arabidopsis thaliana; (iii) inbreeding tolerance enabling development of recombinant inbred lines, near-isogenic lines and positional cloning; (iv) interspecific crosses permitting mapping for genetic analysis of speciation; (v) apomixis (asexual reproduction by seeds) in a genetically tractable diploid; and (vi) broad geographic distribution in North America, permitting ecological genetics for a large research community. These characteristics, along with the current sequencing of three Boechera species by the Joint Genome Institute, position Boechera as a rapidly advancing system for EEFG studies.     

Hybridization in Trypanosoma congolense does not challenge the predominant clonal evolution model. A comment on Tihon et al., 2017, Mol. Ecol.

Tihon et al. have just published in Mol. Ecol. a fine genomic study on Trypanosoma congolense, agent of Animal African Trypanosomiasis. They present very convincing evidence that T. congolense underwent several hybridization events between distinct genetic lines in Zambia. They claim that their data challenge our predominant clonal evolution model (PCE) of micropathogens. We point out the main tenets of our model and show that Tihon et al.'s claim is based on a misinterpretation of the PCE model. Actually, their data strongly support PCE in T. congolense at a microevolutionary level.     

metapop2: Re‐implementation of software for the analysis and management of subdivided populations using gene and allelic diversity

Management programmes often have to make decisions based on the analysis of the genetic properties and diversity of populations. Expected heterozygosity (or gene diversity) and population structure parameters are often used to make recommendations for conservation, such as avoidance of inbreeding or migration across subpopulations. Allelic diversity, however, can also provide complementary and useful information for conservation programmes, as it is highly sensitive to population bottlenecks, and is more related to long‐term selection response than heterozygosity. Here we present a completely revised and updated re‐implementation of the software metapop for the analysis of diversity in subdivided populations, as well as a tool for the management and dynamic estimation of optimal contributions in conservation programmes. This new update includes computation of allelic diversity for population analysis and management, as well as a simulation mode to forecast the consequences of taking different management strategies over time. Furthermore, the new implementation in C++ includes code optimization and improved memory usage, allowing for fast analysis of large data sets including single nucleotide polymorphism markers, as well as enhanced cross‐software and cross‐platform compatibility.     

Back to basics: using colour polymorphisms to study evolutionary processes

Here, I suggest that colour polymorphic study systems have been underutilized to answer general questions about evolutionary processes, such as morph frequency dynamics between generations and population divergence in morph frequencies. Colour polymorphisms can be used to study fundamental evolutionary processes like frequency‐dependent selection, gene flow, recombination and correlational selection for adaptive character combinations. However, many previous studies of colour polymorphism often suffer from weak connections to population genetic theory. I argue that too much focus has been directed towards noticeable visual traits (colour) at the expense of understanding the evolutionary processes shaping genetic variation and covariation associated with polymorphisms in general. There is thus no need for a specific evolutionary theory for colour polymorphisms beyond the general theory of the maintenance of polymorphisms in spatially or temporally variable environments or through positive or negative frequency‐dependent selection. I outline an integrative research programme incorporating these processes and suggest some fruitful avenues in future investigations of colour polymorphisms.     

Widespread hybridization and bidirectional introgression in sympatric species of coral reef fish

Coral reefs are highly diverse ecosystems, where numerous closely related species often coexist. How new species arise and are maintained in these high geneflow environments have been long‐standing conundrums. Hybridization and patterns of introgression between sympatric species provide a unique insight into the mechanisms of speciation and the maintenance of species boundaries. In this study, we investigate the extent of hybridization between two closely related species of coral reef fish: the common coral trout (Plectropomus leopardus) and the bar‐cheek coral trout (Plectropomus maculatus). Using a complementary set of 25 microsatellite loci, we distinguish pure genotype classes from first‐ and later‐generation hybrids, identifying 124 interspecific hybrids from a collection of 2,991 coral trout sampled in inshore and mid‐shelf reefs of the southern Great Barrier Reef. Hybrids were ubiquitous among reefs, fertile and spanned multiple generations suggesting both ecological and evolutionary processes are acting to maintain species barriers. We elaborate on these finding to investigate the extent of genomic introgression and admixture from 2,271 SNP loci recovered from a ddRAD library of pure and hybrid individuals. An analysis of genomic clines on recovered loci indicates that 261 SNP loci deviate from a model of neutral introgression, of which 132 indicate a pattern of introgression consistent with selection favouring both hybrid and parental genotypes. Our findings indicate genome‐wide, bidirectional introgression between two sympatric species of coral reef fishes and provide further support to a growing body of evidence for the role of hybridization in the evolution of coral reef fishes.     

Homomorphic plant sex chromosomes are coming of age

Sex chromosomes are a very peculiar part of the genome that have evolved independently in many groups of animals and plants (Bull 1983 ). Major research efforts have so far been focused on large heteromorphic sex chromosomes in a few animal and plant species (Chibalina & Filatov 2011 ; Zhou & Bachtrog 2012 ; Bellott et al. 2014 ; Hough et al. 2014 ; Zhou et al. 2014 ), while homomorphic (cytologically indistinguishable) sex chromosomes have largely been neglected. However, this situation is starting to change. In this issue, Geraldes et al. ( 2015 ) describe a small (~100 kb long) sex‐determining region on the homomorphic sex chromosomes of poplars (Populus trichocarpa and related species, Fig.  1 ). All species in Populus and its sister genus Salix are dioecious, suggesting that dioecy and the sex chromosomes, if any, should be relatively old. Contrary to this expectation, Geraldes et al. ( 2015 ) demonstrate that the sex‐determining region in poplars is of very recent origin and probably evolved within the genus Populus only a few million years ago.     

Genetic variation and asexual reproduction in the facultatively parthenogenetic cockroach Nauphoeta cinerea: implications for the evolution of sex

Asexual reproduction could offer up to a two‐fold fitness advantage over sexual reproduction, yet higher organisms usually reproduce sexually. Even in facultatively parthenogenetic species, where both sexual and asexual reproduction is sometimes possible, asexual reproduction is rare. Thus, the debate over the evolution of sex has focused on ecological and mutation‐elimination advantages of sex. An alternative explanation for the predominance of sex is that it is difficult for an organism to accomplish asexual reproduction once sexual reproduction has evolved. Difficulty in returning to asexuality could reflect developmental or genetic constraints. Here, we investigate the role of genetic factors in limiting asexual reproduction in Nauphoeta cinerea, an African cockroach with facultative parthenogenesis that nearly always reproduces sexually. We show that when N. cinerea females do reproduce asexually, offspring are genetically identical to their mothers. However, asexual reproduction is limited to a nonrandom subset of the genotypes in the population. Only females that have a high level of heterozygosity are capable of parthenogenetic reproduction and there is a strong familial influence on the ability to reproduce parthenogenetically. Although the mechanism by which genetic variation facilitates asexual reproduction is unknown, we suggest that heterosis may facilitate the switch from producing haploid meiotic eggs to diploid, essentially mitotic, eggs.     

Beauty in the eyes of the beholders: colour vision is tuned to mate preference in the Trinidadian guppy (Poecilia reticulata)

A broad range of animals use visual signals to assess potential mates, and the theory of sensory exploitation suggests variation in visual systems drives mate preference variation due to sensory bias. Trinidadian guppies (Poecilia reticulata), a classic system for studies of the evolution of female mate choice, provide a unique opportunity to test this theory by looking for covariation in visual tuning, light environment and mate preferences. Female preference co‐evolves with male coloration, such that guppy females from ‘low‐predation’ environments have stronger preferences for males with more orange/red coloration than do females from ‘high‐predation’ environments. Here, we show that colour vision also varies across populations, with ‘low’‐predation guppies investing more of their colour vision to detect red/orange coloration. In independently colonized watersheds, guppies expressed higher levels of both LWS‐1 and LWS‐3 (the most abundant LWS opsins) in ‘low‐predation’ populations than ‘high‐predation’ populations at a time that corresponds to differences in cone cell abundance. We also observed that the frequency of a coding polymorphism differed between high‐ and low‐predation populations. Together, this shows that the variation underlying preference could be explained by simple changes in expression and coding of opsins, providing important candidate genes to investigate the genetic basis of female preference variation in this model system.     

Soft selection reduces loss of heterozygosity in asexual reproduction

The adaptive value of sexual reproduction is still debated in evolutionary theory. It has been proposed that the advantage of sexual reproduction over asexual reproduction is to promote genetic diversity, to prevent the accumulation of harmful mutations or to preserve heterozygosity. Since these hypothetical advantages depend on the type of asexual reproduction, understanding how selection affects the taxonomic distribution of each type could help us discriminate between existing hypotheses. Here, I argue that soft selection, competition among embryos or offspring in selection arenas prior to the hard selection of the adult phase, reduces loss of heterozygosity in certain types of asexual reproduction. Since loss of heterozygosity leads to the unmasking of recessive deleterious mutations in the progeny of asexual individuals, soft selection facilitates the evolution of these types of asexual reproduction. Using a population genetics model, I calculate how loss of heterozygosity affects fitness for different types of apomixis and automixis, and I show that soft selection significantly reduces loss of heterozygosity, hence increases fitness, in apomixis with suppression of the first meiotic division and in automixis with central fusion, the most common types of asexual reproduction. Therefore, if sexual reproduction evolved to preserve heterozygosity, soft selection should be associated with these types of asexual reproduction. I discuss the evidence for this prediction and how this and other observations on the distribution of different types of asexual reproduction in nature is consistent with the heterozygosity hypothesis.     

Isolation of polymorphic microsatellite loci from the red‐billed gull (Larus novaehollandiae scopulinus) and amplification in related species

We describe the isolation and characterization of seven dinucleotide microsatellite loci developed from the red‐billed gull (Larus novaehollandiae scopulinus). Locus‐specific primers were used to genotype individuals from 13 populations of this subspecies as well as individuals from closely related subspecies from Australia and New Caledonia. The primers were tested successfully on other species of gulls and shorebirds. The number of alleles observed within the red‐billed gull ranged from three to 17, and observed heterozygosity varied from 0.359 to 0.787. These microsatellites are likely to be useful for studies of mating systems and population genetics in a wide range of gull species.     

Inversions are bigger on the X chromosome

In many insects, X‐linked inversions fix at a higher rate and are much less polymorphic than autosomal inversions. Here, we report that in Drosophila, X‐linked inversions also capture 67% more genes. We estimated the number of genes captured through an approximate Bayesian computational analysis of gene orders in nine species of Drosophila. X‐linked inversions fixed with a significantly larger gene content. Further, X‐linked inversions of intermediate size enjoy highest fixation rate, while the fixation rate of autosomal inversions decreases with size. A less detailed analysis in Anopheles suggests a similar pattern holds in mosquitoes. We develop a population genetic model that assumes the fitness effects of inversions scale with the number of genes captured. We show that the same conditions that lead to a higher fixation rate also produce a larger size for inversions on the X.     

Genetic evidence for a recent origin by hybridization of red wolves

Genetic data suggest that red wolves ( Canis rufus ) resulted from a hybridization between coyotes ( C. latrans ) and grey wolves ( C. lupus ). The date of the hybridization, however, is uncertain. According to one hypothesis, the two species came into contact as coyotes increased their geographical range in conjunction with the advance of European settlers and as grey wolves were extirpated from the American south. Alternatively, the red wolves could have originated tens of thousands of years ago as a result of climate and habitat changes that disturbed the ecology of the two parent species. To obtain an upper limit on the date of hybridization that would help to distinguish the two scenarios, we compared microsatellite allele length distributions from red wolves, coyotes and grey wolves. Subject to the assumptions of our analysis, we conclude that the red wolves originated as a result of hybridizations that occurred during the past 12 800 years, and probably during the past 2500 years.     

megasat: automated inference of microsatellite genotypes from sequence data

megasat is software that enables genotyping of microsatellite loci using next‐generation sequencing data. Microsatellites are amplified in large multiplexes, and then sequenced in pooled amplicons. megasat reads sequence files and automatically scores microsatellite genotypes. It uses fuzzy matches to allow for sequencing errors and applies decision rules to account for amplification artefacts, including nontarget amplification products, replication slippage during PCR (amplification stutter) and differential amplification of alleles. An important feature of megasat is the generation of histograms of the length–frequency distributions of amplification products for each locus and each individual. These histograms, analogous to electropherograms traditionally used to score microsatellite genotypes, enable rapid evaluation and editing of automatically scored genotypes. megasat is written in Perl, runs on Windows, Mac OS X and Linux systems, and includes a simple graphical user interface. We demonstrate megasat using data from guppy, Poecilia reticulata. We genotype 1024 guppies at 43 microsatellites per run on an Illumina MiSeq sequencer. We evaluated the accuracy of automatically called genotypes using two methods, based on pedigree and repeat genotyping data, and obtained estimates of mean genotyping error rates of 0.021 and 0.012. In both estimates, three loci accounted for a disproportionate fraction of genotyping errors; conversely, 26 loci were scored with 0–1 detected error (error rate ≤0.007). Our results show that with appropriate selection of loci, automated genotyping of microsatellite loci can be achieved with very high throughput, low genotyping error and very low genotyping costs.     

Inbreeding avoidance and female mate choice shape reproductive skew in capuchin monkeys (Cebus capucinus imitator)

Reproductive skew in multimale groups may be determined by the need for alpha males to offer reproductive opportunities as staying incentives to subordinate males (concessions), by the relative fighting ability of the alpha male (tug‐of‐war) or by how easily females can be monopolized (priority‐of‐access). These models have rarely been investigated in species with exceptionally long male tenures, such as white‐faced capuchins, where female mate choice for novel unrelated males may be important in shaping reproductive skew. We investigated reproductive skew in white‐faced capuchins at Sector Santa Rosa, Costa Rica, using 20 years of demographic, behavioural and genetic data. Infant survival and alpha male reproductive success were highest in small multimale groups, which suggests that the presence of subordinate males can be beneficial to the alpha male, in line with the concession model's assumptions. None of the skew models predicted the observed degree of reproductive sharing, and the probability of an alpha male producing offspring was not affected by his relatedness to subordinate males, whether he resided with older subordinate males, whether he was prime aged, the number of males or females in the group or the number of infants conceived within the same month. Instead, the alpha male's probability of producing offspring decreased when he was the sire of the mother, was weak and lacked a well‐established position and had a longer tenure. Because our data best supported the inbreeding avoidance hypothesis and female choice for strong novel mates, these hypotheses should be taken into account in future skew models.     

Maintenance of a genetic polymorphism by fluctuating selection on sex‐limited traits

Fluctuating selection is often thought to be ineffective in maintaining a genetic polymorphism except when generations overlap, for example when a seed bank causes a storage effect. Here, I demonstrate that fluctuating selection on sex‐limited traits automatically includes such a ‘storage effect’ because sex‐limited alleles are shielded from selection in the sex where they are not expressed. With analytical calculations and numerical simulations I show that fluctuating selection can maintain a genetic polymorphism in sex‐limited traits. Such a protected polymorphism can reduce the cost of sex when female‐limited traits are involved. But, this effect will probably be small compared to the two‐fold advantage of asexual reproduction unless many polymorphic loci interact or exceptionally strong environmental fluctuations are present. It is argued that genetic polymorphisms maintained by fluctuating selection on sex‐limited traits may partly explain the large genetic variance of traits under strong sexual selection.     

Love the one you're with: proximity determines paternity success in the barnacle Tetraclita rubescens

A species' mating system sets limits on the strength of sexual selection. Sexual selection is widespread in dioecious species, but is less well documented in hermaphrodites, and may be less important. We used four highly polymorphic microsatellite markers to assign paternity to broods of the hermaphroditic eastern Pacific volcano barnacle Tetraclita rubescens. These data were used to describe the species' mating system and to examine factors affecting male reproductive success. Tetraclita can sire broods over distances of 11.2 cm, but proximity to the sperm recipient had a highly significant effect on the probability of siring success. There was no effect of body size or the mass of male reproductive tissues on siring success. Broods showed relatively low frequencies of multiple paternity; even at high densities, 75% of broods had only one father. High frequencies of single‐paternity broods imply either that this species does not compete via sperm displacement, or that sperm displacement is extremely effective, potentially explaining the lack of a positive relationship between male investment and paternity. In addition, there was low variance in siring success among individuals, suggesting a lack of strong sexual selection on male traits. Low variance among sires and the strong effect of proximity are probably driven by the unusual biology of a sessile copulating species.