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.     

Genital damage in the orb-web spider Argiope bruennichi (Araneae: Araneidae) increases paternity success

The morphology of male genitalia often suggests functions besidessperm transfer that may have evolved under natural or sexualselection. In several species of sexually cannibalistic spiders,males damage their paired genitalia during mating, limitingthem to one copulation per pedipalp. Using a triple-mating experiment,we tested if genital damage in the orb-web spider Argiope bruennichiincreases male fitness either through facilitating his escapefrom an aggressive female or by obstructing the female's inseminationducts against future copulation attempts from other males. Wefound no survival advantage for males damaging their pedipalps;however, copulations into a previously used insemination ductwere significantly shorter when the previous male had left partsof his genitalia inside the insemination duct. Because copulationduration determines paternity in this species, our result suggeststhat male genital damage in A. bruennichi is sexually selected.By breaking off parts of their intromittent organs inside avirgin female, males can reduce sperm competition and therebyincrease their paternity success.     

Maintenance of androdioecy in the freshwater shrimp Eulimnadia texana: sexual encounter rates and outcrossing success

The clam shrimp Eulimnadia texana has a rare mating system known as androdioecy, in which males and hermaphrodites cooccur butthere are no pure females. In this species, reproduction takesplace by outcrossing between males and hermaphrodites, or byselfing within a hermaphrodite; this system provides a uniqueopportunity to examine the adaptive significance of out-crossingand selfing in animals. Our study examined mating behavior in hermaphrodites and males from two populations to understandthe propensity of these shrimp to mate and to estimate a parameterof a model developed by Otto et al. (American Naturalist 141:329-337),which predicts the conditions for stability of the mixed matingsystem in E. texana. Here we present evidence that mating frequencyis environmentally sensitive, with greater numbers of encountersand matings per male when males are rare and in younger males.However, the effects of shrimp density, relative male frequency,and shrimp age interact in a complex way to determine malemating success. Overall, mating frequency was determined bya combination of encounter rates between the sexes and theproportion of encounters resulting in mating. The mating rateswere then used to estimate one of four parameters of the Ottoet al. model, and these estimates were combined with previousestimates of the other three parameters to examine the fitof the predicted to the observed sex ratios in the two populations.     

Correlated paternity measures mate monopolization and scales with the magnitude of sexual selection

Indirect measures of sexual selection have been criticized because they can overestimate the magnitude of selection. In particular, they do not account for the degree to which mating opportunities can be monopolized by individuals of the sex that compete for mates. We introduce a measure of mate monopolization (m) based on the magnitude of correlated paternity and evaluate its ability to track changes in the magnitude of sexual selection. Simulation models were used to compare how well m tracked changes in the selection differential (s) for a trait regulating mating success. We further evaluated the association between m and s using ten replicate mating arrays of Sagittaria latifolia in which plants with contrasting alleles at microsatellite loci competed for siring opportunities. The computer models and mating arrays both demonstrated a positive linear association between m and s, supporting the utility of m as an index of sexual selection. Commonly used measures of sexual selection are not easily applied to organisms, such as the flowering plants, for which mating events are difficult to observe. The measure of mate monopolization introduced here could prove to be a useful addition to studies of sexual selection in these organisms.     

The relative role of relatives in conspecific brood parasitism

Conspecific brood parasites lay their eggs in the nests of other females in the same population, leading to a fascinating array of possible ‘games’ among parasites and their hosts ( Davies 2000 ; Lyon & Eadie 2008 ). Almost 30 years ago, Andersson & Eriksson (1982) first suggested that perhaps this form of parasitism was not what it seemed—indeed, perhaps it was not parasitism at all! Andersson & Eriksson (1982) observed that conspecific brood parasitism (CBP) was disproportionally common in waterfowl (Anatidae), a group of birds for which natal philopatry is female‐biased rather than the more usual avian pattern of male‐biased natal philopatry. Accordingly, Andersson (1984) reasoned (and demonstrated in an elegantly simple model) that relatedness among females might facilitate the evolution of CBP—prodding us to reconsider it as a kin‐selected and possibly cooperative breeding system rather than a parasitic interaction. The idea was much cited but rarely tested empirically until recently—a number of new studies, empowered with a battery of molecular techniques, have now put Andersson’s hypothesis to the test ( Table 1 ). The results are tantalizing, but also somewhat conflicting. Several studies, focusing on waterfowl, have found clear evidence that hosts and parasites are often related ( Andersson & Åhlund 2000 ; Roy Nielsen et al. 2006 ; Andersson & Waldeck 2007 ; Waldeck et al. 2008 ; Jaatinen et al. 2009 ; Tiedemann et al. 2011 ). However, this is not always the case ( Semel & Sherman 2001 ; Anderholm et al. 2009 ; and see Pöysa 2004 ). In a new study reported in this issue of Molecular Ecology, Jaatinen et al. (2011a) provide yet another twist to this story that might explain not only why such variable results have been obtained, but also suggests that the games between parasites and their hosts—and the role of kinship in these games—may be even more complex than Andersson (1984) imagined. Indeed, the role of kinship in CBP may be very much one of relative degree!

Table 1. A summary of recent studies that have tested for evidence of relatedness between hosts and parasites in avian conspecific brood parasites

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.     

Genetic covariance between components of male reproductive success: within‐pair vs. extra‐pair paternity in song sparrows

The evolutionary trajectories of reproductive systems, including both male and female multiple mating and hence polygyny and polyandry, are expected to depend on the additive genetic variances and covariances in and among components of male reproductive success achieved through different reproductive tactics. However, genetic covariances among key components of male reproductive success have not been estimated in wild populations. We used comprehensive paternity data from socially monogamous but genetically polygynandrous song sparrows (Melospiza melodia) to estimate additive genetic variance and covariance in the total number of offspring a male sired per year outside his social pairings (i.e. his total extra‐pair reproductive success achieved through multiple mating) and his liability to sire offspring produced by his socially paired female (i.e. his success in defending within‐pair paternity). Both components of male fitness showed nonzero additive genetic variance, and the estimated genetic covariance was positive, implying that males with high additive genetic value for extra‐pair reproduction also have high additive genetic propensity to sire their socially paired female's offspring. There was consequently no evidence of a genetic or phenotypic trade‐off between male within‐pair paternity success and extra‐pair reproductive success. Such positive genetic covariance might be expected to facilitate ongoing evolution of polygyny and could also shape the ongoing evolution of polyandry through indirect selection.     

Preliminary analysis of reproductive success in a large mammal with alternative mating tactics,the Northern chamois,Rupicapra rupicapra

In polygynous mating systems, reproductive skew depends on the ability of males to monopolize females, which in turn may promote the development of contrasting traits in the two sexes. Although dominant individuals normally enjoy a higher reproductive success (RS) than subordinates, the use of genetic markers has shown that behavioural observations of male mating success may not provide reliable clues of RS. We report the preliminary results of the first DNA‐based paternity analysis on the Northern chamois (Rupicapra rupicapra), a scarcely dimorphic mountain ungulate described as highly polygynous, in relation to mating tactic and age. Because of sampling difficulties, the success in parentage assignment was low, and the interpretation of results requires caution. Territorial males had a greater RS than nonterritorial ones but they were unable to monopolize mating events. Age had a weak effect on paternity outcome but only males ≥ 6 years showed siring success. Although future studies are needed to assess the opportunity for sexual selection in male chamois, the concurrence of limited sexual size dimorphism, compensatory growth, unbiased sex‐specific survival, RS of alternative mating tactics and, possibly, long breeding tenure, may hint at the adoption of a conservative mating strategy in this species.     

Male reproductive success in a promiscuous mammal: behavioural estimates compared with genetic paternity

Molecular techniques have enabled behavioural ecologists to reassess mating systems from a genetic perspective. Studies of paternity frequently reveal that mating behaviour does not always reflect parentage, and may bring to light alternative mating tactics. Here we present a comparison of behavioural and genetic measures of male reproductive success in a mammalian mating system in which both sexes are highly promiscuous. Rather than having a stable harem social structure, Soay rams (Ovis aries) on the island of Hirta, St Kilda, UK usually consort with individual oestrous ewes sequentially. Not all matings occur between consort pairs, however, and ewes have been seen to mate with up to 10 different rams on the same day. Using locus-specific polymorphism at five protein and 10 microsatellite DNA loci, we determined paternity for 236 lambs born into three cohorts, and compared paternity with estimates of mating success derived from more than one census of rutting behaviour. The correlation between the number of ewes with which each ram was witnessed in consort and the number of paternities assigned was positive and statistically significant, and rams that were observed in consort with a ewe were 18 times more likely to have sired her offspring than other candidate rams. However, most lambs (73%) were not sired by a ram seen in consort with the oestrous mother. Many juveniles, yearlings and some adult rams were rarely seen in consort with ewes, yet were assigned a significant number of paternities. These results suggest that mating tactics differ between age groups, and that alternative mating strategies among adults that do not involve forming consorts with many females also confer mating success. For these reasons, census-based observations of consort associations between individuals cannot be used to accurately estimate individual male reproductive success in this population.     

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.     

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.     

Securing paternity: mating plugs in the dwarf spider Oedothorax retusus (Araneae: Erigoninae)

One of the various male strategies to prevent or impede female remating is the production of a mating plug that covers the female genital opening or remains inside of the female genital tract after mating. Such structures have been described for many species in many animal taxa; however, in most cases, we know little or nothing about their specific adaptive value. Our investigations demonstrate that females of the dwarf spider species Oedothorax retusus (Westring, 1851) (Linyphiidae, Erigoninae) exhibit a substance on one or both of her paired genital openings only after copulation. We performed double-mating trials and forced the second male to mate into the previously used or unused spermathecal duct of the female by amputating one of his paired male gonopods (pedipalps). Furthermore, to investigate whether the duration of the first mating has an effect on the size and efficiency of the mating plug, we interrupted first matings after either 1 or 3 min, categorized plug size and recorded mating behaviour of subsequent males. The amount of secretion transferred was larger in long compared to short copulations. A long first copulation successfully prevented subsequent males from mating into the used ducts, whereas mating success after short first matings was similar to matings into unused copulatory ducts of the females. The present study demonstrates that a male O. retusus can prevent a rival from transferring sperm into the same spermatheca by applying a mating plug, but only if he mates for long enough.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 574–583.     

Blue and green egg-color intensity is associated with parental effort and mating system in passerines: support for the sexual selection hypothesis

Among several adaptive explanations proposed to account for variation in avian egg color, that related to sexual selection is of particular interest because of its possible generality. Briefly, it proposes that because biliverdin (the pigment responsible for blue-green eggshell coloration) is an antioxidant, deposition in the eggshell by laying females may signal the capacity of females to control free radicals, despite the handicap of removing this antioxidant from their body. If males adjust parental effort in response to the intensity of the blue coloration of eggs, thereby investing more in the offspring of high-quality mates, blue eggs may represent a postmating sexually selected signal in females. Here, by image and spectrophotometric analyses of the eggs of European passerines, we tested two different predictions of the hypothesis. First, variables related to intraspecific variation in parental effort (i.e., the duration of the nestling period controlled for body mass) should be positively related to the intensity of blue-green color of the eggshell across species. Second, there should be a positive relationship between intensity of blue-green color of eggs and degree of polygyny. These predictions were supported: intensity of blue-green coloration (i.e., chroma) was significantly related to the duration of the nestling period and to degree of polygyny after controlling for possible confounding variables (i.e., body mass, incubation period, and nest type) and similarity due to common descent. Nest type (hole or nonhole) also explained a significant proportion of variation in egg chroma, perhaps reflecting different selection pressures (i.e., light conditions, risk of parasitism) affecting species with the two types of nests.     

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.     

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.     

Size and mating success in males of the western harvester ant,Pogonomyrmex occidentalis (Hymenoptera: Formicidae)

Mating success in males of the lek mating ant species,Pogonomyrmex occidentalis, increases with increased body size. We estimated the magnitude of the selection coefficients on components of size by collecting males in copula and comparing their morphology to that of males that were collected at the lek but that were not mating. Four characters, body mass, head width, wing length, and leg length, were measured for a sample of 225 mating and 324 nonmating males and 225 females. Significant direct selection favors increased wing length and leg length. Multiple regression of transformed variables (principal components) indicated that the increased mating success of larger males is a function of all four characters. We found no evidence of positive assortative mating on the basis of any individual character or on the multivariate general size variable (the first principal component).     

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.     

Unravelling the evolution of complex reproductive traits with phenotypic engineering

The social dynamics surrounding courtship, mating and parental care are complex enough when just a single male and female are involved, but for species that employ multiple strategies for achieving fertilization success, the network of interactions among rivals, allies and suitors can be utterly complicated. Such is the case in the ocellated wrasse, Symphodus ocellatus, in which males adopt one of three mating strategies. The large, colourful “nesting males” court females, defend territories and care for fertilized eggs until they hatch. The smaller “satellite males” help the nesting males court females and guard against the third morph, the “sneaker males”, which sneak in when a nesting male is spawning with a female and surreptitiously release sperm. Sneaker males perform no courtship displays nor defend territories, so their reproductive investment is devoted entirely to sperm production. And these alternative male strategies work: 100% of nests contain some eggs fertilized by sneaker and satellite males, despite the fact that parental care is solely the responsibility of nesting males In this issue of Molecular Ecology, work to untangle the proximate mechanisms regulating the reproductive physiology of nesting males and their behaviour towards other males, which impacts the entire social network. Moreover, they describe how variation in neuroendocrine regulation can give rise to variation in reproductive traits, upon which sexual selection can act.