scholarly journals Inter-genomic sexual conflict drives antagonistic coevolution in harvester ants

2014 ◽  
Vol 281 (1797) ◽  
pp. 20141771
Author(s):  
Michael Herrmann ◽  
Sara Helms Cahan

The reproductive interests of males and females are not always aligned, leading to sexual conflict over parental investment, rate of reproduction and mate choice. Traits that increase the genetic interests of one sex often occur at the expense of the other, selecting for counter-adaptations leading to antagonistic coevolution. Reproductive conflict is not limited to intraspecific interactions; interspecific hybridization can produce pronounced sexual conflict between males and females of different species, but it is unclear whether such conflict can drive sexually antagonistic coevolution between reproductively isolated genomes. We tested for hybridization-driven sexually antagonistic adaptations in queens and males of the socially hybridogenetic ‘J’ lineages of Pogonomyrmex harvester ants, whose mating system promotes hybridization in queens but selects against it in males. We conducted no-choice mating assays to compare patterns of mating behaviour and sperm transfer between inter- and intra-lineage pairings. There was no evidence for mate discrimination on the basis of pair type, and the total quantity of sperm transferred did not differ between intra- and inter-lineage pairs; however, further dissection of the sperm transfer process into distinct mechanistic components revealed significant, and opposing, cryptic manipulation of copulatory investment by both sexes. Males of both lineages increased their rate of sperm transfer to high-fitness intra-lineage mates, with a stronger response in the rarer lineage for whom mating mistakes are the most likely. By contrast, the total duration of copulation for intra-lineage mating pairs was significantly shorter than for inter-lineage crosses, suggesting that queens respond to prevent excessive sperm loading by prematurely terminating copulation. These findings demonstrate that sexual conflict can lead to antagonistic coevolution in both intra-genomic and inter-genomic contexts. Indeed, the resolution of sexual conflict may be a key determinant of the long-term evolutionary potential of host-dependent reproductive strategies, counteracting the inherent instabilities arising from such systems.

Author(s):  
Rachel Olzer ◽  
Rebecca L. Ehrlich ◽  
Justa L. Heinen-Kay ◽  
Jessie Tanner ◽  
Marlene Zuk

Sex and reproduction lie at the heart of studies of insect behavior. We begin by providing a brief overview of insect anatomy and physiology, followed by an introduction to the overarching themes of parental investment, sexual selection, and mating systems. We then take a sequential approach to illustrate the diversity of phenomena and concepts behind insect reproductive behavior from pre-copulatory mate signalling through copulatory sperm transfer, mating positions, and sexual conflict, to post-copulatory sperm competition, and cryptic female choice. We provide an overview of the evolutionary mechanisms driving reproductive behavior. These events are linked by the economic defendability of mates or resources, and how these are allocated in each sex. Under the framework of economic defendability, the reader can better understand how sexual antagonistic behaviors arise as the result of competing optimal fitness strategies between males and females.


2017 ◽  
Vol 86 (3) ◽  
pp. 229-237 ◽  
Author(s):  
Xin Tong ◽  
Lu Jiang ◽  
Bao-Zhen Hua

Sexually reproductive insects exhibit diverse mating behaviors. However, the mating pattern remains unknown for Panorpodes of Panorpodidae to date. In this study, we investigated the mating behavior and copulatory mechanism of the short-faced scorpionfly Panorpodes kuandianensis Zhong, Zhang and Hua, 2011 for the first time. The results show that the male provides a salivary mass as a nuptial gift to the female and starts to copulate with the female in a V-shaped position, then changes to an end-to-end position by temporarily twisting the female abdominal segments VII−IX by 180°. During mating the basal processes and the basal teeth of the gonostyli and the hypandrium are used to obtain copulation and sustain the coupling of genitalia to secure successful sperm transfer. This unique mating pattern is greatly different from that of other Mecoptera reported and is likely evolved as an adaptation in the context of sexual conflict.


2020 ◽  
Vol 75 (1) ◽  
Author(s):  
Julia A. Kunz ◽  
Guilhem J. Duvot ◽  
Maria A. van Noordwijk ◽  
Erik P. Willems ◽  
Manuela Townsend ◽  
...  

Abstract Sexual coercion, in the form of forced copulations, is relatively frequently observed in orangutans and generally attributed to their semi-solitary lifestyle. High ecological costs of association for females may be responsible for this lifestyle and may have prevented the evolution of morphological fertility indicators (e.g., sexual swellings), which would attract (male) associates. Therefore, sexual conflict may arise not only about mating per se but also about associations, because males may benefit from associations with females to monitor their reproductive state and attempt to monopolize their sexual activities. Here, we evaluate association patterns and costs for females when associating with both males and females of two different orangutan species at two study sites: Suaq, Sumatra (Pongo abelii), and Tuanan, Borneo (Pongo pygmaeus wurmbii). Female association frequency with both males and females was higher in the Sumatran population, living in more productive habitat. Accordingly, we found that the cost of association, in terms of reduced feeding to moving ratio and increased time being active, is higher in the less sociable Bornean population. Males generally initiated and maintained such costly associations with females, and prolonged associations with males led to increased female fecal cortisol metabolite (FCM) levels at Tuanan, the Bornean population. We conclude that male-maintained associations are an expression of sexual conflict in orangutans, at least at Tuanan. For females, this cost of association may be responsible for the lack of sexual signaling, while needing to confuse paternity. Significance statement Socioecological theory predicts a trade-off between the benefits of sociality and the ecological costs of increased feeding competition. Orangutans’ semi-solitary lifestyle has been attributed to the combination of high association costs and low predation risk. Previous work revealed a positive correlation between association frequencies and habitat productivity, but did not measure the costs of association. In this comparative study, we show that females likely incur costs from involuntary, male-maintained associations, especially when they last for several days and particularly in the population characterized by lower association frequencies. Association maintenance therefore qualifies as another expression of sexual conflict in orangutans, and especially prolonged, male-maintained associations may qualify as an indirect form of sexual coercion.


2006 ◽  
Vol 361 (1466) ◽  
pp. 363-374 ◽  
Author(s):  
Tristan A.F Long ◽  
Robert Montgomerie ◽  
Adam K Chippindale

Six sister populations of Drosophila melanogaster kept under identical environmental conditions for greater than 600 generations were reciprocally crossed to investigate the incidence of population divergence in allopatry. Population crosses directly influenced fitness, mating frequency, and sperm competition patterns. Changes in both female remating rate and the outcome of male sperm competition (P 1 , P 2 ) in response to foreign males were consistent with intersexual coevolution. Moreover, seven of the 30 crosses between foreign mates resulted in significant reductions in female fitness, whereas two resulted in significant increases, compared to local matings. This tendency for foreign males to reduce female fitness may be interpreted as evidence for either sexually antagonistic coevolution or the disruption of mutualistic interactions. However, instances in which female fitness improved via cohabitation with foreign males may better reveal sexual conflict, signalling release from the cost of interacting with locally adapted males. By this metric, female reproduction in D. melanogaster is strongly constrained by local adaptation by males, a situation that would promote antagonistic coevolution between the sexes. We conclude that sexual selection can promote population differentiation in allopatry and that sexual conflict is likely to have played a role in population differentiation in this study system.


2018 ◽  
Author(s):  
Devon E. Pearse ◽  
Nicola J. Barson ◽  
Torfinn Nome ◽  
Guangtu Gao ◽  
Matthew A. Campbell ◽  
...  

AbstractTraits with different fitness optima in males and females cause sexual conflict when they have a shared genetic basis. Heteromorphic sex chromosomes can resolve this conflict and protect sexually antagonistic polymorphisms but accumulate deleterious mutations. However, many taxa lack differentiated sex chromosomes, and how sexual conflict is resolved in these species is largely unknown. Here we present a chromosome-anchored genome assembly for rainbow trout (Oncorhynchus mykiss) and characterize a 56 Mb double-inversion supergene that mediates sex-specific migration through sex-dependent dominance, a mechanism that reduces sexual conflict. The double-inversion contains key photosensory, circadian rhythm, adiposity, and sexual differentiation genes and displays frequency clines associated with latitude and temperature, revealing environmental dependence. Our results constitute the first example of sex-dependent dominance across a large autosomal supergene, a novel mechanism for sexual conflict resolution capable of protecting polygenic sexually antagonistic variation while avoiding the homozygous lethality and deleterious mutation load of heteromorphic sex chromosomes.


Behaviour ◽  
2015 ◽  
Vol 152 (14) ◽  
pp. 1883-1910 ◽  
Author(s):  
Peter Morse ◽  
Kyall R. Zenger ◽  
Mark I. McCormick ◽  
Mark G. Meekan ◽  
Christine L. Huffard

The southern blue-ringed octopus,Hapalochlaena maculosaHoyle (1883), is a nocturnal species that exhibits a mating system in which females hold sperm from multiple males over a one to two month breeding window before laying a single egg clutch. Contrary to most studied animal mating systems where anisogamy exists, gamete package production is limited for both males and females of this species (approx. 50 spermatophores/eggs). This presents an animal model for studying aspects of sperm competition and dynamic mate choice behaviours. The present study reports on the mating behaviour ofH. maculosaobserved under laboratory conditions using infrared closed-circuit television video footage. Rates of male copulation attempts increased with male size, while female receptivity to mating attempts increased with female size, resulting in larger animals of both sexes gaining more copulations and spending more time per day in copulation. There was some evidence of female preference of larger males, but no male preference of females based on measured morphological traits. Both sexes terminated copulations in equal frequencies but male-terminated copulations were significantly shorter in duration. Males were more likely to terminate copulation early with females they had previously mated with, however were less likely to do so if the female had recently mated with a different male. Among male-terminated copulations, males mated for longer with females that had previously mated with other males in the trial. Male–male mounts were as common as male–female mounts, suggesting that maleH. maculosaare not able to discriminate the sex of conspecifics. These findings suggest male strategic allocation of spermatophores based female mating history is an important factor influencing mating behaviours of this species.


2020 ◽  
Vol 375 (1813) ◽  
pp. 20200069 ◽  
Author(s):  
Jonathan P. Evans ◽  
Rowan A. Lymbery

Broadcast spawning invertebrates offer highly tractable models for evaluating sperm competition, gamete-level mate choice and sexual conflict. By displaying the ancestral mating strategy of external fertilization, where sexual selection is constrained to act after gamete release, broadcast spawners also offer potential evolutionary insights into the cascade of events that led to sexual reproduction in more ‘derived’ groups (including humans). Moreover, the dynamic reproductive conditions faced by these animals mean that the strength and direction of sexual selection on both males and females can vary considerably. These attributes make broadcast spawning invertebrate systems uniquely suited to testing, extending, and sometimes challenging classic and contemporary ideas in sperm competition, many of which were first captured in Parker's seminal papers on the topic. Here, we provide a synthesis outlining progress in these fields, and highlight the burgeoning potential for broadcast spawners to provide both evolutionary and mechanistic understanding into gamete-level sexual selection more broadly across the animal kingdom. This article is part of the theme issue ‘Fifty years of sperm competition’.


2016 ◽  
Vol 113 (8) ◽  
pp. E978-E986 ◽  
Author(s):  
Tanya M. Pennell ◽  
Freek J. H. de Haas ◽  
Edward H. Morrow ◽  
G. Sander van Doorn

Evolutionary conflict between the sexes can induce arms races in which males evolve traits that are detrimental to the fitness of their female partners, and vice versa. This interlocus sexual conflict (IRSC) has been proposed as a cause of perpetual intersexual antagonistic coevolution with wide-ranging evolutionary consequences. However, theory suggests that the scope for perpetual coevolution is limited, if traits involved in IRSC are subject to pleiotropic constraints. Here, we consider a biologically plausible form of pleiotropy that has hitherto been ignored in treatments of IRSC and arrive at drastically different conclusions. Our analysis is based on a quantitative genetic model of sexual conflict, in which genes controlling IRSC traits have side effects in the other sex, due to incompletely sex-limited gene expression. As a result, the genes are exposed to intralocus sexual conflict (IASC), a tug-of-war between opposing male- and female-specific selection pressures. We find that the interaction between the two forms of sexual conflict has contrasting effects on antagonistic coevolution: Pleiotropic constraints stabilize the dynamics of arms races if the mating traits are close to evolutionary equilibrium but can prevent populations from ever reaching such a state. Instead, the sexes are drawn into a continuous cycle of arms races, causing the buildup of IASC, alternated by phases of IASC resolution that trigger the next arms race. These results encourage an integrative perspective on the biology of sexual conflict and generally caution against relying exclusively on equilibrium stability analysis.


2015 ◽  
Vol 282 (1804) ◽  
pp. 20143063 ◽  
Author(s):  
Kazuki Kimura ◽  
Satoshi Chiba

Several taxa of simultaneously hermaphroditic land snails exhibit a conspicuous mating behaviour, the so-called shooting of love darts. During mating, such land snail species transfer a specific secretion by stabbing a mating partner's body with the love dart. It has been shown that sperm donors benefit from this traumatic secretion transfer, because the secretions manipulate the physiology of a sperm recipient and increase the donors' fertilization success. However, it is unclear whether reception of dart shooting is costly to the recipients. Therefore, the effect of sexual conflict and antagonistic arms races on the evolution of traumatic secretion transfer in land snails is still controversial. To examine this effect, we compared lifetime fecundity and longevity between the individuals that received and did not receive dart shooting from mating partners in Bradybaena pellucida . Our experiments showed that the dart-receiving snails suffered reduction in lifetime fecundity and longevity. These results suggest that the costly mating behaviour, dart shooting, generates conflict between sperm donors and recipients and that sexually antagonistic arms races have contributed to the diversification of the morphological and behavioural traits relevant to dart shooting. Our findings also support theories suggesting a violent escalation of sexual conflict in hermaphroditic animals.


Sign in / Sign up

Export Citation Format

Share Document