Sexual conflict occurs because males and females are exposed to different selection pressures. This can affect many aspects of female and male biology, such as physiology, behavior, genetics, and even population ecology. Its broad impact has caused widespread interest in sexual conflict. However, a key aspect of sexual conflict is often confused; it comprises two distinct forms: intralocus and interlocus sexual conflict (IASC and IRSC). Although both are caused by sex differences in selection, they operate via different proximate and ultimate mechanisms. Intralocus sexual conflict and IRSC are often not clearly defined as separate processes in the scientific literature, which impedes a proper understanding of each form as well as of their relative impact on sexual conflict. Furthermore, our current knowledge of the genetics of these phenomena is severely limited. This prevents us from empirically testing numerous theories regarding the role of these two forms of sexual conflict in evolution. Here, we clarify the distinction between IASC and IRSC, by discussing how male and female interests differ, how and when sex‐specific adaptation occurs, and how this may lead to evolutionary change. We then describe a framework for their study, focusing on how future experiments may help identify the genetics underlying these phenomena. Through this, we hope to promote a more critical reflection on IASC and IRSC as well as underline the necessity of genetic and mechanistic studies of these two phenomena.

Heritable microbial symbionts have profound impacts upon the biology of their arthropod hosts. Whilst our current understanding of the dynamics of these symbionts is typically cast within a framework of vertical transmission only, horizontal transmission has been observed in a number of cases. For instance, several symbionts can transmit horizontally when their parasitoid hosts share oviposition patches with uninfected conspecifics, a phenomenon called superparasitism. Despite this, horizontal transmission, and the host contact structures that facilitates it, have not been considered in heritable symbiont epidemiology. Here, we tested for the importance of host contact, and resulting horizontal transmission, for the epidemiology of a male-killing heritable symbiont (Arsenophonus nasoniae) in parasitoid wasp hosts. We observed that host contact through superparasitism is necessary for this symbiont’s spread in populations of its primary host Nasonia vitripennis, such that when superparasitism rates are high, A. nasoniae almost reaches fixation, causes highly female biased population sex ratios and consequently causes local host extinction. We further tested if natural interspecific variation in superparasitism behaviours predicted symbiont dynamics among parasitoid species. We found that A. nasoniae was maintained in laboratory populations of a closely related set of Nasonia species, but declined in other, more distantly related pteromalid hosts. The natural proclivity of a species to superparasitise was the primary factor determining symbiont persistence. Our results thus indicate that host contact behaviour is a key factor for heritable microbe dynamics when horizontal transmission is possible, and that ‘reproductive parasite’ phenotypes, such as male-killing, may be of secondary importance in the dynamics of such symbiont infections. Most insects house heritable symbionts and these represent an important component of their biology, both as partners conveying beneficial traits such as defence against natural enemies, or as antagonists manipulating their hosts’ reproduction. Work on these bacteria mostly assumes that such phenotypes have evolved primarily to facilitate the symbiont’s vertical transmission from parent to offspring. However, several such bacteria also move horizontally between unrelated individuals. Here, we show that a male-killing symbiont actually depends upon horizontal transmission for its spread and maintenance. We observed Arsenophonus nasoniae was only maintained in parasitoid wasp populations when the route enabling horizontal transmission, superparasitism of fly pupae, was allowed. When superparasitism was common enough to cause epidemic spread of A. nasoniae, host population extinction occurred due to lack of males. Our study indicates that superparasitism behaviour is likely to be the key element determining which wasp species maintain this symbiont in nature. This provides new insights into the factors determining heritable symbiont frequency within and amongst species, and highlights the extreme effects such symbionts can have on their host populations. The data also indicate that male-killing may evolve and be maintained as an additional, rather than primary, driver of heritable symbiont fitness.

The paradox of the organism refers to the observation that organisms appear to function as coherent purposeful entities, despite the potential for within‐organismal components like selfish genetic elements and cancer cells to erode them from within. While it is commonly accepted that organisms may pursue fitness maximisation and can be thought to hold particular agendas, there is a growing recognition that genes and cells do so as well. This can lead to evolutionary conflicts between an organism and the parts that reside within it. Here, we revisit the paradox of the organism. We first outline its conception and relationship to debates about adaptation in evolutionary biology. Second, we review the ways selfish elements may exploit organisms, and the extent to which this threatens organismal integrity. To this end, we introduce a novel classification scheme that distinguishes between selfish elements that seek to distort transmission versus those that seek to distort phenotypic traits. Our classification scheme also highlights how some selfish elements elude a multi‐level selection decomposition using the Price equation. Third, we discuss how the organism can retain its status as the primary fitness‐maximising agent in the face of selfish elements. The success of selfish elements is often constrained by their strategy and further limited by a combination of fitness alignment and enforcement mechanisms controlled by the organism. Finally, we argue for the need for quantitative measures of both internal conflicts and organismality.

Sex determination (SD) is a crucial developmental process, but its molecular underpinnings are very diverse, both between and within species. SD mechanisms have traditionally been categorized as either genetic (GSD) or environmental (ESD), depending on the type of cue that triggers sexual differentiation. However, mixed systems, with both genetic and environmental components, are more prevalent than previously thought. Here, we show theoretically that environmental effects on expression levels of genes within SD regulatory mechanisms can easily trigger within-species evolutionary divergence of SD mechanisms. This may lead to the stable coexistence of multiple SD mechanisms and to spatial variation in the occurrence of different SD mechanisms along environmental gradients. We applied the model to the SD system of the housefly, a global species with world-wide latitudinal clines in the frequencies of different SD systems, and found that it correctly predicted these clines if specific genes in the housefly SD system were assumed to have temperature-dependent expression levels. We conclude that environmental sensitivity of gene regulatory networks may play an important role in diversification of SD mechanisms.

Complementary sex determination (CSD) is a widespread sex determination mechanism in haplodiploid Hymenoptera. Under CSD, sex is determined by the allelic state of one or multiple CSD loci. Heterozygosity at one or more loci leads to female development, whereas hemizygosity of haploid eggs and homozygosity of diploid eggs results in male development. Sexual (arrhenotokous) reproduction normally yields haploid male and diploid female offspring. Under asexual reproduction (thelytoky), diploidized unfertilized eggs develop into females. Thelytoky is often induced by bacterial endosymbionts that achieve egg diploidization by gamete duplication. As gamete duplication leads to complete homozygosity, endosymbiont‐induced thelytokous reproduction is presumed to be incompatible with CSD, which relies on heterozygosity for female development. Previously, we excluded CSD in fourAsobara(Braconidae) species and proposed a two‐step mechanism forWolbachia‐induced thelytoky inAsobara japonica. Here, we conclusively reject CSD in two cynipid wasp species,Leptopilina heterotomaandLeptopilina clavipes. We further show that thelytoky inL. clavipesdepends onWolbachiatiter but that diploidization and feminization steps cannot be separated, unlike inA. japonica. We discuss what these results reveal about the sex determination mechanism ofL. clavipesand the presumed incompatibility between CSD and endosymbiont‐induced thelytoky in the Hymenoptera.

Houseflies provide a good experimental model to study the initial evolutionary stages of a primary sex-determining locus because they possess different recently evolved proto-Y chromosomes that contain male-determining loci (M) with the same male-determining gene, Mdmd. We investigate M-loci genomically and cytogenetically revealing distinct molecular architectures among M-loci. M on chromosome V (M^V) has two intact Mdmd copies in a palindrome. M on chromosome III (M^III) has tandem duplications containing 88 Mdmd copies (only one intact) and various repeats, including repeats that are XY-prevalent. M on chromosome II (M^II) and the Y (M^Y) share M^III-like architecture, but with fewer repeats. M^Y additionally shares M^V-specific sequence arrangements. Based on these data and karyograms using two probes, one derives from M^III and one Mdmd-specific, we infer evolutionary histories of polymorphic M-loci, which have arisen from unique translocations of Mdmd, embedded in larger DNA fragments, and diverged independently into regions of varying complexity.