Sexual selection under parental choice: the role of parents in the evolution of human mating

Much of the evolutionary literature on human mating is based on the assumption of extensive female choice during the history of our species. However, ethnographic evidence from foraging societies reveals that, in societies thought to be akin to those of our ancestors, female choice is constrained by the control that parents exercise over their daughters. Data from 190 hunting and gathering societies indicate that almost all reproduction takes place while the woman is married and that the institution of marriage is regulated by parents and close kin. Parents are able to influence the mating decisions of both sons and daughters, but stronger control is exercised with regard to daughters; male parents have more say in selecting in-laws than their female counterparts. In light of the fact that parental control is the typical pattern of mate choice among extant foragers, it is likely that this pattern was also prevalent throughout human evolution. Because daughters' preferences can be expected not to fully coincide with those of their parents, research to date may thus have simultaneously overestimated the contribution of female preferences to processes of sexual selection and underestimated the contribution of parental preferences to such processes.     

Confounding social and mating systems predictably lead to biased results when examining the evolution of cooperative breeding in cichlids: A response to Tanaka et al.

In 2017, we demonstrated that transitions to cooperative breeding in Lamprologine cichlid fishes were not related to a species’ social mating system (Dey et al. 2017. Nature Ecology & Evolution, 1 , 137). This contrasted previous evidence that monogamy (and a low degree of promiscuity) promoted transitions to cooperative breeding in other taxa. Recently, Tanaka et al. (2018. Ethology, 124 , 777–789) critiqued our study and argued that a re‐analysis of the data shows transitions to cooperative breeding are promoted by non‐monogamous mating systems. Here, we show that Tanaka et al.'s critique contains numerous inaccuracies. In addition, we show that the results put forth by Tanaka et al. emerge only under the extreme scenario in which all cooperative breeding species are classified as non‐monogamous, which we argue arises because Tanaka et al. confound social systems and mating systems. While we agree that there is uncertainty regarding the mating system of some Lamprologine species, we argue this uncertainty was sufficiently addressed through the extensive sensitivity analyses conducted in our original study.     

Results for generalized regular inbreeding systems

A probabilistic and algebraic treatment of regular inbreeding systems was introduced in Arzberger (1985). In that paper it was shown that (1) regular inbreeding systems can be thought of as graphs of certain semigroups, (2) these graphs reflect a certain natural homogeneity property, (3) a sufficient condition for the population to become genetically uniform is GS 1/A _r diverges, where A _r is the number of ancestors r generations into the past. In this paper, a specific class of inbreeding systems is studied. For this class, the results of the previous paper are extended to generalized regular inbreeding systems in which overlapping generations in the mating scheme are allowed. A new result about the structure of the set of ancestors of two individuals is presented.     

Space Use and Social Mating System of the Hantavirus Host, <Emphasis Type="Italic">Oligoryzomys longicaudatus</Emphasis>

The long-tailed mouse, Oligoryzomys longicaudatus (Cricetidae: Sigmodontinae), is the major host of Andes hantavirus, the etiological agent of hantavirus pulmonary syndrome in the south of Argentina and Chile. Studying the ecology of this species is necessary to understand how Andes hantavirus is maintained in nature. In this study, we examine the home range size and intra- and intersexual overlap degree of male and female O. longicaudatus in order to elucidate the mating system of this species. To our knowledge, this research provides the first documentation, obtained from a specific design, of spacing and mating systems in this species in Argentina. The study was conducted seasonally from April (autumn) 2012 to October (spring) 2013 in a shrubland habitat of Cholila, Andean region, Argentina. We studied spacing patterns using 59 and 51 home ranges established by adult males and females, respectively, in two 3.24 ha capture-marked and recapture grids. Significant differences between sexes in home range size and overlap degree were found. Male home ranges were always larger than those of females. We observed exclusive space use both among males and females (13.15 ± 18.67, and 3.60 ± 3.43%, respectively). Considering only those males that get access to receptive females (40%), average intersexual overlap value was about 30.82 ± 19.73%. Sexual differences in home range sizes and the spatial avoidance between breeding males, that would reflect intrasexual competition for receptive females, allows us to propose a polygynous mating system for O. longicaudatus.     

Raising Darwin’s consciousness

Sociobiologists and feminists agree that men in patriarchal social systems seek to control females, but sociobiologists go further, using Darwin’s theory of sexual selection and Trivers’s ideas on parental investment to explain why males should attempt to control female sexuality. From this perspective, the stage for the development under some conditions of patriarchal social systems was set over the course of primate evolution. Sexual selection encompasses both competition between males and female choice. But in applying this theory to our “lower origins” (prehominid ancestors), Darwin assumed that choices were made by essentially “coy” females. I argue here that female solicitation of multiple males (either simultaneously or sequentially, depending on the breeding system) characterized prehominid females; this prehominid legacy of cyclical sexual assertiveness, itself possibly a female counter-strategy to male efforts to control the timing of female reproduction, generated further male counter-strategies. This dialectic had important implications for emerging hominid mating systems, human evolution, and the development of patriarchal arrangements in some human societies. For hominid males who will invest in offspring, there would be powerful selection for emotions, behaviors, and customs that ensure them certainty of paternity. The sexual modesty that so struck Darwin can be explained as a recent evolved or learned (perhaps both) adaptation in women to avoid penalties imposed by patrilines on daughters and mates who failed to conform to the patriline’s prevailing norms for their sex. Other supposedly innate universals, such as female preferences for wealthy husbands, are also likely to be facultative accommodations by women to constraints set up when patrilines monopolized resources needed by females to survive and reproduce, and passed on intergenerational control of these resources preferentially to sons.     

Promiscuous mating in the harem-roosting fruit bat, Cynopterus sphinx

Observations on mating behaviours and strategies guide our understanding of mating systems and variance in reproductive success. However, the presence of cryptic strategies often results in situations where social mating system is not reflective of genetic mating system. We present such a study of the genetic mating system of a harem-forming bat Cynopterus sphinx where harems may not be true indicators of male reproductive success. This temporal study using data from six seasons on paternity reveals that social harem assemblages do not play a role in the mating system, and variance in male reproductive success is lower than expected assuming polygynous mating. Further, simulations reveal that the genetic mating system is statistically indistinguishable from promiscuity. Our results are in contrast to an earlier study that demonstrated high variance in male reproductive success. Although an outcome of behavioural mating patterns, standardized variance in male reproductive success (I(m)) affects the opportunity for sexual selection. To gain a better understanding of the evolutionary implications of promiscuity for mammals in general, we compared our estimates of I(m) and total opportunity for sexual selection (I(m) /I(f), where I(f) is standardized variance in female reproductive success) with those of other known promiscuous species. We observed a broad range of I(m) /I(f) values across known promiscuous species, indicating our poor understanding of the evolutionary implications of promiscuous mating.     

Mating schemes for optimum contribution selection with constrained rates of inbreeding

The effect of non-random mating on genetic response was compared for populations with discrete generations. Mating followed a selection step where the average coancestry of selected animals was constrained, while genetic response was maximised. Minimum coancestry (MC), Minimum coancestry with a maximum of one offspring per mating pair (MC1) and Minimum variance of the relationships of offspring (MVRO) mating schemes resulted in a delay in inbreeding of about two generations compared with Random, Random factorial and Compensatory mating. In these breeding schemes where selection constrains the rate of inbreeding, ΔF, the improved family structure due to non-random mating increased genetic response. For schemes with ΔF constrained to 1.0% and 100 selection candidates, genetic response was 22% higher for the MC1 and MVRO schemes compared with Random mating schemes. For schemes with a less stringent constraint on ΔF or more selection candidates, the superiority of the MC1 and MVRO schemes was smaller (5–6%). In general, MC1 seemed to be the preferred mating method, since it almost always yielded the highest genetic response. MC1 mainly achieved these high genetic responses by avoiding extreme relationships among the offspring, i.e. fullsib offspring are avoided, and by making the contributions of ancestors to offspring more equal by mating least related animals.     

The mating system of the brown bear Ursus arctos

• 1 Research on mating systems and reproductive strategies is valuable for providing ethological knowledge, important for the management and conservation of a species, and in a broader sense, important for biodiversity conservation.
• 2 We reviewed the literature to document the mating system of the brown bear Ursus arctos. We determined that many aspects of the reproduction of the brown bear remain unclear, including (i) biological aspects, such as hormone and oestrous cycling, sperm competition, mate choice, sexually selected infanticide, etc. and (ii) human impacts on the mating system, occurring when humans alter population size and structure, through, for example, hunting or habitat degradation.
• 3 We considered three mating system classification frameworks from the literature ( Emlen & Oring 1977 , Clutton‐Brock 1989 , Shuster & Wade 2003 ) and applied various brown bear populations to them. We did this (i) to document the plasticity of the mating system of the brown bear, and (ii) to find commonalities among the reported mating system classifications in order to provide a general and common classification of the brown bear's mating system.
• 4 The mating system of the brown bear can, in general, be classed as ‘polygamous’. Subclassifications can nevertheless be valuable on smaller spatial scales.
• 5 Within the polygamous mating system of the brown bear, biological aspects and human impacts can influence reproductive strategies at the individual and population level. Mating system classification frameworks often lack a common terminology, which contributes to the variety of published classifications of the mating system of the brown bear.

     

The structure and measurement of human mating strategies: toward a multidimensional model of sociosexuality

Recent theoretical perspectives concerning the structure of variation in human mating have focused less on conceptualizations of alternate mating strategies and more on the evolution of a conditional strategy. Empirical evidence suggests that this conditional strategy may involve the simultaneous pursuit of long-term and short-term mating tactics. Despite these developments, empirical measurement has proceeded using the Sociosexual Orientation Inventory (SOI), which measures restricted and unrestricted mating orientations along a single bipolar continuum. To fully capture the pluralistic nature of human mating, we suggest that a multidimensional empirical measure is required. To test our hypothesis, we subjected an expanded version of the SOI, which included items measuring psychological orientation toward short-term mating and long-term mating, to principal components analysis. A three-factor structure representing short-term mating orientation, long-term mating orientation, and previous sexual behavior emerged. In subsequent analyses, we demonstrate that our newly developed long-term and short-term dimensions (a) are largely independent and (b) correlate differentially with other theoretically relevant variables.     

广东罗坑自然保护区饲养鳄蜥的求偶和交配行为

半自然条件下,通过直接观察及影像分析法对鳄蜥(Shinisaurss crocodilurus)的求偶和交配行为进行了研究.共记录了20种与鳄蜥求偶和交配有关的行为,其求偶和交配行为的一般模式为:(1)炫耀;(2)接近;(3)舔舐;(4)咬颈;(5)环抱;(6)交媾;(7)分离.该行为过程的持续时间分别为(157.29±33.81)s、(15.57±1.59)8、(10.86±3.05)s、(169.28±31.99)s、(66.14±16.08)s、(2 417.14±229.30)s和(26.86±9.15)s.鳄蜥的婚配制度可能是多雄多雌的婚配制,其求偶和交配模式与其近缘类群相似.     

Analysis of the localization of STE6/CFTR chimeras in a Saccharomyces cerevisiae model for the cystic fibrosis defect CFTRΔF508

The use of yeast as a model system to study mammalian proteins is attractive, because yeast genetic tools can be utilized if a suitable phenotype is created. STE6, the Saccharomyces cerevisiae a-factor mating pheromone transporter, and CFTR, the mammalian cystic fibrosis transmembrane conductance regulator, are both members of the ATP binding cassette (ABC) superfamily. Teem et al . (1993) described a yeast model for studying a mutant form of the cystic fibrosis protein, CFTRΔF508. The model involved expression of a chimeric molecule in which a portion of yeast STE6 was replaced with the corresponding region from mammalian CFTR. The STE6/CFTR chimera complemented a ste6 mutant strain for mating, indicating that it could export a-factor. However, mating efficiency was dramatically reduced upon introduction of ΔF508, providing a yeast phenotype for this mutation. In human cells, the ΔF508 mutation results in retention of CFTR in the endoplasmic reticulum (ER), and possibly in reduction of its chloride-channel activity. Here we examine the basis for the differences in STE6 activity promoted by the wild-type and mutant STE6/CFTR chimeras. By analysis of protein stability and subcellular localization, we find that the mutant chimera is not ER-retained in yeast. We conclude that the molecular basis for the reduced mating of the STE6/CFTRΔF508 chimera must reflect a reduction in its capacity to transport a-factor, rather than mistrafficking. Thus, STE6/CFTRΔF508 in yeast appears to be a good genetic model to probe certain aspects of protein function, but not to study protein localization.     

The unexpected genetic mating system of the red‐backed toadlet (Pseudophryne coriacea): A species with prolonged terrestrial breeding and cryptic reproductive behaviour

Molecular technologies have revolutionized our classification of animal mating systems, yet we still know very little about the genetic mating systems of many vertebrate groups. It is widely believed that anuran amphibians have the highest reproductive diversity of all vertebrates, yet genetic mating systems have been studied in <1% of all described species. Here, we use single nucleotide polymorphisms to quantify the genetic mating system of the terrestrial breeding red‐backed toadlet Pseudophryne coriacea. In this species, breeding is prolonged (approximately 5 months), and males construct subterranean nests in which females deposit eggs. We predicted that females would display extreme sequential polyandry because this mating system has been reported in a closely related species (P. bibronii). Parentage analysis revealed that mating success was heavily skewed towards a subset of males (30.6% of potential sires) and that nearly all females (92.6%) mated with one male. In a high percentage of occupied nests (37.1%), the resident male was not the genetic sire, and very few nests (4.3%) contained clutches with multiple paternity. Unexpectedly, these results show that sequential polyandry is rare. They also show that there is a high frequency of nest takeover and extreme competition between males for nest sites, but that males rarely sneak matings. Genetic analysis also revealed introgressive hybridization between P. coriacea and the red‐crowned toadlet (Pseudophryne australis). Our study demonstrates a high level of mating system complexity, and it shows that closely related anurans can vary dramatically in their genetic mating system.     

Altered mating behaviour in a Cry1Ac-resistant strain of Helicoverpa armigera (Lepidoptera: Noctuidae)

Randomness of mating between susceptible and resistant individuals is a major factor that closely relates to the refuge strategy of resistance management for Helicoverpa armigera (Hübner) to Bacillus thuringiensis cotton. The mating behaviour of Cry1Ac‐susceptible and Cry1Ac‐resistant strains of H. armigera was compared to investigate the randomness of their mating. The percentage of mating was lower for Cry1Ac‐resistant H. armigera compared with that of the susceptible strain under both no‐choice and multiple‐choice conditions. The low percentage of mating in the resistant strain indicates a reduced incidence of successful mating. The percentage of spermatophore‐containing mated female H. armigera in the crossing of susceptible females × resistant males was significantly lower than in the crossing of resistant females × susceptible males, but the observed mating frequencies of these two types of cross were similar to each other. This indicates that resistant males reduce the incidence of mating paternity more than they do their mating frequency. The percentages of heterogametic matings (susceptible females × resistant males, resistant females × susceptible males) in the multiple‐choice experiment were lower than those of homogametic matings (susceptible × susceptible, resistant × resistant) on peak mating nights. However, the difference between heterogametic and homogametic mating was not significant, indicating that there was a random mating between susceptible and resistant strains. The results presented here do not reflect reality in mating associated with Cry1Ac resistance but can provide insight into variable expression.     

Emergence and mating behavior of the oriental fruit moth Cydia molesta (Lepidoptera: Tortricidae) and its potential for reproduction

The Oriental fruit moth, Cydia molesta (Busck, 1916) (Lepidoptera: Tortricidae), is a key pest of fruit and is widely distributed around the world. There are important connections between its behavior and biology and its management in agriculture, but few studies have investigated the associations between adult behaviors and oviposition. In this study, adult emergence, mating, and reproduction were investigated under laboratory and field conditions. The ratio of females to males at eclosion was approximately 1:1. When one virgin female had access to one virgin male, 66% and 34% of the couples copulated just once and twice, respectively; and the infertility rate of eggs (21.39 ± 1.25%) did not vary daily. Males, given access to one new female daily, could copulate multiple times, whereas females seldom mated more than once, indicating a male-biased operational sex ratio, but mating status of the male parent had no effect on progeny egg reproduction. Also, the number of eggs that hatched by all female partners of a male was inversely proportional to copulation duration for the female laying the eggs for total female reproductive success; and the number of eggs laid by all female partners of a male was proportional to their number of matings for total male reproductive success. However, the total number of eggs that hatched did not significantly differ for eggs laid by a female given new virgin males daily for mating (17.75 ± 4.28) versus eggs laid by virgin females (19.17 ± 7.51) presented daily with a male that re-mated daily with the series of females. Therefore, our results showed that females engaged in mate choice and males engaged in mate competition, affecting egg production, a factor that may be used to enhance mating disruption technology against Cydia molesta.     

Comportements reproducteurs du labre oiseau Gomphosus caeruleus dans un récif de l’île de la Réunion : mode de reproduction,facteurs environnementaux et alternance des stratégies reproductrices

The green birdmouth wrasse Gomphosus caeruleus is present all year round on the coral reefs of Reunion Island (Indian Ocean). A group of individuals was followed on one of these reefs with the objective of studying the reproduction mode of the species, the influence of environmental factors, and social behaviors on the control of reproduction. Our observations revealed that G. caeruleus is, like many Labridae, a protogynous hermaphrodite species, probably diandric, that the reproduction of G. caeruleus is, like in other reef fish species, influenced by the lunar cycle with a peak of reproductive activity during waxing gibbous phase, and that G. caeruleus displays social behavior leading to alternating haremic mating system on a single territory and lek-like mating systems without aggressions between males. These observations enhanced our knowledge of the reproduction of Labridae and reef species.     

Experimental evolution of mating discrimination in budding yeast

Assortative mating, when individuals of similar phenotypes mate, likely plays a key role in preventing gene flow during speciation. Reinforcement occurs when two previously geographically separated (allopatric) groups meet after having evolved partial postzygotic isolation; they are selected to evolve or enhance assortative mating to prevent costly intergroup matings that produce only maladaptive or sterile hybrids. Studies in Drosophila have shown that the genetic architectures of mating discrimination could differ significantly with or without reinforcement, suggesting that the evolution of assortative mating may be more complicated than expected. To study the evolution of assortative mating, we evolved mating discrimination in populations of the budding yeast, Saccharomyces cerevisiae. After 36 cycles of selection, these cells are five times more likely to mate with each other than to their ancestors, despite detectable one-way gene flow between the selected and reference populations. Several individual cultures evolved mating discrimination by changing their mating kinetics, with some mating more rapidly and others more slowly than the ancestral population. Genetic analysis indicates that multiple mutations have accumulated to produce the altered mating preference. Our results show that subtle details of mating behavior can play an important role in the evolution of reproductive isolation.     

Sexual selection targets cetacean pelvic bones

Male genitalia evolve rapidly, probably as a result of sexual selection. Whether this pattern extends to the internal infrastructure that influences genital movements remains unknown. Cetaceans (whales and dolphins) offer a unique opportunity to test this hypothesis: since evolving from land‐dwelling ancestors, they lost external hind limbs and evolved a highly reduced pelvis that seems to serve no other function except to anchor muscles that maneuver the penis. Here, we create a novel morphometric pipeline to analyze the size and shape evolution of pelvic bones from 130 individuals (29 species) in the context of inferred mating system. We present two main findings: (1) males from species with relatively intense sexual selection (inferred by relative testes size) tend to evolve larger penises and pelvic bones compared to their body length, and (2) pelvic bone shape has diverged more in species pairs that have diverged in inferred mating system. Neither pattern was observed in the anterior‐most pair of vertebral ribs, which served as a negative control. This study provides evidence that sexual selection can affect internal anatomy that controls male genitalia. These important functions may explain why cetacean pelvic bones have not been lost through evolutionary time.     

Inbreeding avoidance behaviors

Inbreeding is defined as mating between individuals related by common ancestry. Thus, the degree to which a particular mating is inbred depends on how far back in a pedigree one begins counting common ancestors. In general practice, the term inbreeding is used to describe mating between close relatives (first cousins or closer). Animal breeders have known for centuries that inbreeding causes a loss of constitutional vigor and fertility in domestic livestock. A growing literature now demonstrates that the offspring of matings between close relatives in species of undomesticated birds and mammals are less fit than outbred offspring. The deleterious consequences of inbreeding suggest the possibility that many species have evolved behaviors that lower the frequency of inbreeding.     

Beyond promiscuity: mate-choice commitments in social breeding

Obligate eusociality with distinct caste phenotypes has evolved from strictly monogamous sub-social ancestors in ants, some bees, some wasps and some termites. This implies that no lineage reached the most advanced form of social breeding, unless helpers at the nest gained indirect fitness values via siblings that were identical to direct fitness via offspring. The complete lack of re-mating promiscuity equalizes sex-specific variances in reproductive success. Later, evolutionary developments towards multiple queen-mating retained lifetime commitment between sexual partners, but reduced male variance in reproductive success relative to female''s, similar to the most advanced vertebrate cooperative breeders. Here, I (i) discuss some of the unique and highly peculiar mating system adaptations of eusocial insects; (ii) address ambiguities that remained after earlier reviews and extend the monogamy logic to the evolution of soldier castes; (iii) evaluate the evidence for indirect fitness benefits driving the dynamics of (in)vertebrate cooperative breeding, while emphasizing the fundamental differences between obligate eusociality and cooperative breeding; (iv) infer that lifetime commitment is a major driver towards higher levels of organization in bodies, colonies and mutualisms. I argue that evolutionary informative definitions of social systems that separate direct and indirect fitness benefits facilitate transparency when testing inclusive fitness theory.     

Human pair‐bonds: Evolutionary functions,ecological variation,and adaptive development

Stable mating relationships are widespread in our species, with important economic, social, and reproductive implications.¹ Pair‐bonds are part of the unique human mosaic, including very large brains, childhood, concealed ovulation, sexual intercourse in private, cultural symbols, and complex social groups. Yet we understand relatively little about the evolution of human pairing, its functions, and consequences for human diversity. We can define pair‐bonds as the long‐term affiliation, including a sexual relationship, between two individuals. The important point is that the union, whether monogamous or polygamous, is relatively enduring. Recent debate about human pair‐bonds highlights apparently conflicting hypotheses: Are pair‐bonds the evolutionary consequence of male mating competition^2,3 or are they an adaptation for paternal provisioning?^4,5 Unfortunately, a simple answer seems unlikely. The evidence indicates selective pressures from both mating competition and provisioning needs, suggesting different benefits of pair‐bonds in different contexts. Whether a bond emphasizes mating or parenting effort may depend on environmental cues. Childhood experience evidently affects pair‐bond development, suggesting further adaptive design for flexible life‐history strategies. © 2008 Wiley‐Liss, Inc.