FEMALE PROMISCUITY IS POSITIVELY ASSOCIATED WITH NEUTRAL AND SELECTED GENETIC DIVERSITY IN PASSERINE BIRDS

Passerine birds show large interspecific variation in extrapair paternity rates. There is accumulating evidence that such promiscuous behavior is driven by indirect, genetic benefits to females. Sexual selection theory distinguishes between two types of genetic benefits, additive and nonadditive effects, mediated by preferences for good and compatible genes, respectively. Good genes preferences should imply directional selection and mating skew among males, and thus reduced genetic diversity in the population. In contrast, compatible genes preferences should give balancing selection that retains genetic diversity. Here, we test how well these predictions fit with patterns of variation in genetic diversity and promiscuity levels among passerine birds. We found that more promiscuous species had higher nucleotide diversity at autosomal introns, but not at Z‐chromosome introns. We also found that major histocompatibility complex (MHC) class IIB alleles had higher sequence diversity, and therefore should recognize a broader spectrum of pathogens, in more promiscuous species. Our results suggest that female promiscuity targets a multitude of autosomal genes for their nonadditive, compatibility benefits. Also, as immunity genes seem to be of particular importance, we hypothesize that interspecific variation in female promiscuity among passerine birds has arisen in response to the strength of pathogen‐mediated selection.     

A comparative study of white blood cell counts and disease risk in carnivores

In primates, baseline levels of white blood cell (WBC) counts are related to mating promiscuity. It was hypothesized that differences in the primate immune system reflect pathogen risks from sexually transmitted diseases (STDs). Here, we test for the generality of this result by examining hypotheses involving behavioural, ecological and life-history factors in carnivores. Again, we find a significant correlation in carnivores between mating promiscuity and elevated levels of WBC counts. In addition, we find relationships with measures of sociality, substrate use and life-history parameters. These comparative results across independent taxonomic orders indicate that the evolution of the immune system, as represented by phylogenetic differences in basal levels of blood cell counts, is closely linked to disease risk involved with promiscuous mating and associated variables. We found only limited support for an association between the percentage of meat in the diet and WBC counts, which is consistent with the behavioural and physiological mechanisms that carnivores use to avoid parasite transmission from their prey. We discuss additional comparative questions related to taxonomic differences in disease risk, modes of parasite transmission and implications for conservation biology.     

A screen for immunity genes evolving under positive selection in Drosophila

Genes involved in the immune system tend to have higher rates of adaptive evolution than other genes in the genome, probably because they are coevolving with pathogens. We have screened a sample of Drosophila genes to identify those evolving under positive selection. First, we identified rapidly evolving immunity genes by comparing 140 loci in Drosophila erecta and D. yakuba. Secondly, we resequenced 23 of the fastest evolving genes from the independent species pair D. melanogaster and D. simulans, and identified those under positive selection using a McDonald-Kreitman test. There was strong evidence of adaptive evolution in two serine proteases (persephone and spirit) and a homolog of the Anopheles serpin SRPN6, and weaker evidence in another serine protease and the death domain protein dFADD. These results add to mounting evidence that immune signalling pathway molecules often evolve rapidly, possibly because they are sites of host-parasite coevolution.     

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.     

Quantifying Adaptive Evolution in the Drosophila Immune System

It is estimated that a large proportion of amino acid substitutions in Drosophila have been fixed by natural selection, and as organisms are faced with an ever-changing array of pathogens and parasites to which they must adapt, we have investigated the role of parasite-mediated selection as a likely cause. To quantify the effect, and to identify which genes and pathways are most likely to be involved in the host–parasite arms race, we have re-sequenced population samples of 136 immunity and 287 position-matched non-immunity genes in two species of Drosophila. Using these data, and a new extension of the McDonald-Kreitman approach, we estimate that natural selection fixes advantageous amino acid changes in immunity genes at nearly double the rate of other genes. We find the rate of adaptive evolution in immunity genes is also more variable than other genes, with a small subset of immune genes evolving under intense selection. These genes, which are likely to represent hotspots of host–parasite coevolution, tend to share similar functions or belong to the same pathways, such as the antiviral RNAi pathway and the IMD signalling pathway. These patterns appear to be general features of immune system evolution in both species, as rates of adaptive evolution are correlated between the D. melanogaster and D. simulans lineages. In summary, our data provide quantitative estimates of the elevated rate of adaptive evolution in immune system genes relative to the rest of the genome, and they suggest that adaptation to parasites is an important force driving molecular evolution.     

田鼠属动物婚配制度的研究范式

从社会组织的生态格局、熟悉性、社会等级和交配近况等择偶行为的影响因子,性二型和雄性射精能力等个体特征,配对关系的神经内分泌机制几方面综述了田鼠动物婚配制度的研究进展,同时从生态学、比较心理学、生理学、神经生物学等方面探讨择偶行类节式的特点。生态学方法,用鼠动物具有完整的婚配制度多样性格局,是婚配制度比较研究的哺乳动物类群。运用比较心理学方法,通过择偶行为实验可直接比较单配制与较研究的理想哺乳动物类     

Adaptation to monogamy influences parental care but not mating behavior in the burying beetle,Nicrophorus vespilloides

The mating system is expected to have an important influence on the evolution of mating and parenting behaviors. Although many studies have used experimental evolution to examine how mating behaviors evolve under different mating systems, this approach has seldom been used to study the evolution of parental care. We used experimental evolution to test whether adaptation to different mating systems involves changes in mating and parenting behaviors in populations of the burying beetle, Nicrophorus vespilloides. We maintained populations under monogamy or promiscuity for six generations. This manipulation had an immediate impact on reproductive performance and adult survival. Compared to monogamy, promiscuity reduced brood size and adult (particularly male) survival during breeding. After six generations of experimental evolution, there was no divergence between monogamous and promiscuous populations in mating behaviors. Parents from the promiscuous populations (especially males) displayed less care than parents from the monogamous populations. Our results are consistent with the hypothesis that male care will increase with the certainty of paternity. However, it appears that this change is not associated with a concurrent change in mating behaviors.     

Sexual Selection and the Molecular Evolution of ADAM Proteins

Rapid evolution has been identified for many reproductive genes and recent studies have combined phylogenetic tests and information on species mating systems to test sexual selection. Here we examined the molecular evolution of the ADAM gene family, a diverse group of 35 proteins capable of adhesion to and cleavage of other proteins, using sequence data from 25 mammalian genes. Out of the 25 genes analyzed, all those expressed in male reproductive tissue showed evidence of positive selection. Positively selected amino acids within the protein adhesion domain were only found in sperm surface ADAM proteins (ADAMs 1, 2, 3, 4, and 32) suggesting selection driven by male × female interactions. We tested heterogeneity in rates of evolution of the adhesion domain of ADAM proteins by using sequence data from Hominidae and macaques. The use of the branch and branch-site models (PAML) showed evidence of higher d _N/d _S and/or positive selection linked to branches experiencing high postmating selective pressures (chimpanzee and macaque) for Adams 2, 18, and 23. Moreover, we found consistent higher proportion of nonsynonymous relative to synonymous and noncoding sequence substitutions in chimpanzee and/or macaque only for Adams 2, 18, and 23. Our results suggest that lineage-specific sexual selection bouts might have driven the evolution of the adhesion sperm protein surface domains of ADAMs 2 and 18 in primates. Adams 2 and 18 are localized in chromosome 8 of primates and adjacent to each other, so their evolution might have also been influenced by their common genome localization.     

A comparative study of leukocyte counts and disease risk in primates

Little is known about how the risk of disease varies across species and its consequences for host defenses, including the immune system. I obtained mean values of basal white blood cells (WBC) from 100 species of primates to quantify disease risk, based on the assumption that higher baseline WBC counts will be found in species that experience greater risk of acquiring infectious disease. These data were used to investigate four hypotheses: disease risk is expected to increase with (1) group size and population density; (2) greater contact with soil-borne pathogens during terrestrial locomotion; (3) a slow life history; and (4) increased mating promiscuity. After controlling for phylogeny, WBC counts increased with female mating promiscuity, as reflected in discrete categories of partner number, relative testes mass, and estrous duration. By comparison, the social, ecological, and life-history hypotheses were unsupported in comparative tests. In terms of confounding variables, some WBC types were associated with body mass or activity period, but these variables could not account for the association with mating promiscuity. Several factors may explain why hypotheses involving social, ecological, and life-history factors went unsupported in these tests, including the role of behavioral counterstrategies to disease, restrictions on female choice of mating partners, and the effect of transmission mode on parasite strategies and host defenses.     

Sequence evolution of the sperm ligand zonadhesin correlates negatively with body weight dimorphism in primates

Sexual selection has repeatedly been shown to be the probable driving force behind the positive Darwinian evolution of genes affecting male reproductive success. Here we compare the sequence evolution of the sperm ligand zonadhesin with body mass dimorphism in primates. In contrast to previous related studies, the present approach takes into account not only catarrhine primates, but also platyrrhines and lemurs. In detail, we analyze the sequence evolution of concatenated zonadhesin fragments (555 bp) of four Lemuroidea, five Platyrrhini, and seven Catarrhini, using the rate ratio of nonsynonymous to synonymous substitutions (dn/ds=omega). Unexpectedly, subsequent regression analyzes between omega estimates for the terminal branches of a primate phylogeny and residual male body mass reveal that sequence evolution of zonadhesin decreases with increasing sexual dimorphism in body weight. Mapping published mating system classifications onto these results illustrates that unimale breeding species show a tendency for rather slow sequence evolution of zonadhesin and comparably pronounced sexual dimorphism in body weight. Female choice and sperm competition can be assumed to drive the evolution of zonadhesin. We speculate that the level of sperm competition is lower in more sexually dimorphic primates because males of these species monopolize access to fertile females more successfully. Thus, variation in sperm competition may be driving the observed negative correlation of sequence evolution and sexual dimorphism in body weight.     

田鼠婚配制度的神经内分泌基础

作为繁殖行为的一种表现形式,婚配制度是通过长期进化而形成的,具有种属特异性及可遗传性。因此,不同的婚配制度具有不同的生理基础。这种生理基础由3级结构组成：神经直接启动并维持繁殖行为;激素或通过诱导特异神经通路的发育或直接激活神经传导影响繁殖行为;基因则可能是通过调节激素的代谢和作用方式来控制与繁殖行为相关的神经系统。田鼠脑中涉及婚配制度的区域集中在视前区中部（MPOA）,腹被盖区（VTA）,膈部及纹状体端部。起作用的激素主要是催产素（OT）和后叶加压素（AVP）。导致田鼠形成不同婚配制度的最终原因可能是这两种激素受体基因上的差异。受体基因调控区的启动子序列存在变异,导致脑中受体基因在表达区域上的差异,进而使激素激活不同的神经通路,产生不同的繁殖行为及婚配制度。     

Is promiscuity associated with enhanced selection on MHC-DQα in mice (genus Peromyscus)?

Reproductive behavior may play an important role in shaping selection on Major Histocompatibility Complex (MHC) genes. For example, the number of sexual partners that an individual has may affect exposure to sexually transmitted pathogens, with more partners leading to greater exposure and, hence, potentially greater selection for variation at MHC loci. To explore this hypothesis, we examined the strength of selection on exon 2 of the MHC-DQα locus in two species of Peromyscus. While the California mouse (P. californicus) is characterized by lifetime social and genetic monogamy, the deer mouse (P. maniculatus) is socially and genetically promiscuous; consistent with these differences in mating behavior, the diversity of bacteria present within the reproductive tracts of females is significantly greater for P. maniculatus. To test the prediction that more reproductive partners and exposure to a greater range of sexually transmitted pathogens are associated with enhanced diversifying selection on genes responsible for immune function, we compared patterns and levels of diversity at the Class II MHC-DQα locus in sympatric populations of P. maniculatus and P. californicus. Using likelihood based analyses, we show that selection is enhanced in the promiscuous P. maniculatus. This study is the first to compare the strength of selection in wild sympatric rodents with known differences in pathogen milieu.     

Z LINKAGE OF FEMALE PROMISCUITY GENES IN THE MOTH UTETHEISA ORNATRIX: SUPPORT FOR THE SEXY‐SPERM HYPOTHESIS?

Female preference genes for large males in the highly promiscuous moth Utetheisa ornatrix (Lepidoptera: Arctiidae) have previously been shown to be mostly Z‐linked, in accordance with the hypothesis that ZZ–ZW sex chromosome systems should facilitate Fisherian sexual selection. We determined the heritability of both female and male promiscuity in the highly promiscuous moth U. ornatrix (Lepidoptera: Arctiidae) through parent–offspring and grandparent–offspring regression analyses. Our data show that male promiscuity is not sex‐limited and either autosomal or sex‐linked whereas female promiscuity is primarily determined by sex‐limited, Z‐linked genes. These data are consistent with the “sexy‐sperm hypothesis,” which posits that multiple‐mating and sperm competitiveness coevolve through a Fisherian‐like process in which female promiscuity is a kind of mate choice in which sperm‐competitiveness is the trait favored in males. Such a Fisherian process should also be more potent when female preferences are Z‐linked and sex‐limited than when autosomal or not limited.     

Decoupling of rapid and adaptive evolution among seminal fluid proteins in heliconius butterflies with divergent mating systems

Reproductive proteins often diverge rapidly between species. This pattern is frequently attributed to postmating sexual selection. Heliconius butterflies offer a good opportunity to examine this hypothesis by contrasting patterns of reproductive protein evolution between clades with divergent mating systems. Pupal-mating Heliconius females typically mate only once, limiting opportunity for postmating sexual selection. In contrast, adult-mating females remate throughout life. Reproductive protein evolution is therefore predicted to be slower and show little evidence of positive selection in the pupal-mating clade. We examined this prediction by sequencing 18 seminal fluid protein genes from a dozen Heliconius species and a related outgroup. Two proteins exhibited dN/dS > 1, implicating positive selection in the rapid evolution of at least a few Heliconius seminal fluid proteins. However, contrary to predictions, the average evolutionary rate of seminal fluid proteins was greater among pupal-mating Heliconius. Based on these results, we suggest that positive selection and relaxed constraint can generate conflicting patterns of reproductive protein evolution between mating systems. As predicted, some loci may show elevated evolutionary rates in promiscuous taxa relative to monandrous taxa resulting from adaptations to postmating sexual selection. However, when monandry is derived (as in Heliconius), the opposite pattern may result from relaxed selective constraints.     

Positive selection on apoptosis related genes

Apoptosis is a form of programmed cell death crucial for development, homeostasis, immunity, spermatogenesis, and prevention of cancer. Positive selection acting on mammalian apoptosis related genes targets protein interfaces that interact with pathogens and also elements of signaling complexes. Selection appears primarily to be driven by the immune/defense related function of these genes. Moreover, competitive interactions could be driving positive selection among sperm cells, as well as the need for protection against female anti-sperm immune responses. Trade-offs in fitness are expected out of these selective pressures, which could explain the involvement of these genes in various diseases, including cancer.     

Paternity and the evolution of male parental care

It is generally believed that level of paternity (the proportion of zygotes in a brood that were fertilized by the male providing parental care) has an important role in the evolution of parental care. We have used population genetics models to investigate this role. The models indicate that only in mating systems where a parental male “sacrifices” promiscous matings can paternity influence the evolution of male parental care. This is because level of paternity can reflect the number of opportunities for these promiscuous fertilizations. For example, high paternity can mean few opportunities and therefore a low cost for paternal care.Certain behaviors may preadapt a species for the evolution of male parental care because they decrease the costs of providing care. For example, in fish species where male care has evolved from spawning territories, the very establishment of territories may have precluded males from gaining promiscuous matings, thereby eliminating the promiscuity costs and facilitating the evolution of care. Without a promiscuity cost, level of paternity will not have influenced the evolution of male care in fishes.Because paternity has limited influence in the evolution of male care, differences in reliability of parentage between males and females are unlikely to explain the prevalence of female care. Our analysis suggests that paternity differences between species cannot serve as a general explanation for the observed patterns of parental care behavior.     

A preliminary study of spatial distribution and mating system of pygmy mouse lemurs (Microcebus cf. myoxinus)

According to current hypotheses on the evolution of life history traits and social systems of Malagasy lemurs, nocturnality is associated with a solitary lifestyle and a polygynous or promiscuous mating system. Recent studies, however, have indicated that this may not be true of all lemurs. The goal of this study was to investigate the sociality and the mating system of pygmy mouse lemurs (Microcebus cf myoxinus), which are the smallest known primates, and which retain characteristics of the most primitive primates. I compared my findings with data on the sympatric Microcebus murinus and Cheirogaleus medius. Observational, morphometric and spatial distribution data were obtained by a radiotracking study in 1994, and from a capture-recapture study conducted during 1995/96. Pygmy mouse lemurs usually slept alone in a tangle of vegetation. During the mating season, sleeping sites of males were distributed over a much broader area than were female sites, indicating that male home ranges are larger than those of females. The home ranges of males overlapped during the mating season, and males occasionally roamed over long distances during a single night. Pygmy mouse lemurs forage primarily alone. Analysis of estrus stages indicate that female cycles are unsynchronized during the mating season. There was a lack of sexual dimorphism in body size but not in body mass. Males were heavier than females during the reproductive season but lighter than females the rest of the year. Testes of males varied in size seasonally and enlarged significantly during the mating season. The presence of a vaginal sperm plug in a female indicated the importance of preventing additional matings in this species. Thus pygmy mouse lemurs follow the predictions derived from sexual selection theory for multi-male mating systems with promiscuous matings and male sperm competition.