100 years of Haldane's rule

Haldane's rule is one of the ‘two rules of speciation’. It states that if one sex is ‘absent, rare or sterile’ in a hybrid population, then that sex will be heterogametic. Since Haldane first made this observation, 100 years have passed and still questions arise over how many independent examples exist and what the underlying causes of Haldane's rule are. This review aims to examine research that has occurred over the last century. It seeks to do so by discussing possible causes of Haldane's rule, as well as gaps in the research of these causes that could be readily addressed today. After 100 years of research, it can be concluded that Haldane's rule is a complicated one, and much current knowledge has been accrued by studying the model organisms of speciation. This has led to the primacy of dominance theory and faster-male theory as explanations for Haldane's rule. However, some of the most interesting findings of the 21st century with regard to Haldane's rule have involved investigating a wider range of taxa emphasizing the need to continue using comparative methods, including ever more taxa as new cases are discovered.     

Genetic dissection of hybrid incompatibilities between Drosophila simulans and D. mauritiana. III. Heterogeneous accumulation of hybrid incompatibilities, degree of dominance, and implications for Haldane's rule

The genetic basis of Haldane's rule was investigated through estimating the accumulation of hybrid incompatibilities between Drosophila simulans and D. mauritiana by means of introgression. The accumulation of hybrid male sterility (HMS) is at least 10 times greater than that of hybrid female sterility (HFS) or hybrid lethality (HL). The degree of dominance for HMS and HL in a pure D. simulans background is estimated as 0.23-0.29 and 0.33-0.39, respectively; that for HL in an F1 background is unlikely to be very small. Evidence obtained here was used to test the Turelli-Orr model of Haldane's rule. Composite causes, especially, faster-male evolution and recessive hybrid incompatibilities, underlie Haldane's rule in heterogametic male taxa such as Drosophila (XY male and XX female). However, if faster-male evolution is driven by sexual selection, it contradicts Haldane's rule for sterility in heterogametic-female taxa such as Lepidoptera (ZW female and ZZ male). The hypothesis of a faster-heterogametic-sex evolution seems to fit the current data best. This hypothesis states that gametogenesis in the heterogametic sex, instead of in males per se, evolves much faster than in the homogametic sex, in part because of sex-ratio selection. This hypothesis not only explains Haldane's rule in a simple way, but also suggests that genomic conflicts play a major role in evolution and speciation.     

Disentangling the benefits of sex

Understanding the evolutionary advantage of sexual reproduction remains one of the most fundamental questions in evolutionary biology. Most of the current hypotheses rely on the fact that sex increases genetic variation, thereby enhancing the efficiency of natural selection; an important body of theoretical work has defined the conditions under which sex can be favoured through this effect. Over the last decade, experimental evolution in model organisms has provided evidence that sex indeed allows faster rates of adaptation. A new study on facultatively sexual rotifers shows that increased rates of sex can be favoured during adaptation to new environmental conditions and explores the cause of this effect. The results provide support for the idea that the benefits of increasing genetic variation may compensate for the short-term costs of sexual reproduction.     

Genetics of postzygotic isolation and Haldane's rule in haplodiploids

The process of speciation has puzzled scientists for decades, but only recently they have they been able to reveal the genetic basis of reproductive isolation. Much emphasis has been on Haldane's rule, the observation that the heterogametic sex often suffers more from hybridization than the homogametic sex. Most research on Haldane's rule has focused on diploid organisms with chromosomal sex determination. We argue that species lacking chromosomal sex determination, such as haplodiploids, also follow Haldane's rule and thus should be included in the definition of this rule. We provide evidence for Haldane's rule in Nasonia wasps and describe how haplodiploids can be used to test the different theories that have been proposed to explain Haldane's rule. We discuss how the faster-male and faster-X theories can shape speciation differently in haplodiploids compared to diploids.     

Dominance and diet are unrelated within a population of invasive crayfish

Laboratory behavioral experiments are an important tool in ecology and evolution, but whether these behaviors reflect the field function of organisms is not always clear. Directly connecting laboratory behaviors to field interactions would increase understanding of a variety of organisms. A recent study proposed using stable isotopes to link laboratory behaviors to field function of individuals, but failed to find any such links within a population of the invasive rusty crayfish Faxonius rusticus (Girard, 1852). Here, we assessed whether methodological decisions around tissue analyzed for stable isotopes, laboratory acclimation time, and timing of primary consumer collection may have affected the result, hypothesizing that more dominant crayfish would have higher trophic positions and tissue with faster turnover rates may exhibit a stronger association between laboratory behavior and recent field function. We tested this relationship using F. rusticus individuals from a single population, and related laboratory dominance to stable isotope-derived trophic position using linear regression. We failed to find a relationship between dominance and trophic position, regardless of our different methodologies. Future studies should consider alternative behaviors that may better relate to function in the field and also investigate whether laboratory behavior and field function are related between, rather than within, populations or species.

     

High thermal variance in naturally incubated turtle nests produces faster offspring

The effects of climate change on populations are complex and difficult to predict, and can result in mismatches between interdependent organisms or between organisms and their environment. Reptiles with temperature-dependent sex determination may be able to compensate for potential skews in offspring sex ratio caused by climate change by selecting cooler (i.e., shadier) nest sites. Although changing nest location may prevent sex ratio skews, it may also affect thermally sensitive performance traits in offspring. I tested righting, sprinting, and swimming performance in hatchling painted turtles (Chrysemys picta), produced by female turtles from five populations across the species’ geographic range, nesting in a common-garden environment. I found that speed of hatchling performance was faster in hatchlings whose mothers originated from warmer climates, and that nests with higher mean daily variation in incubation temperature produced faster hatchlings. These results suggest that the increased temperatures predicted by climate change models could result in hatchling turtles that are faster at sprinting and swimming; however, it is not yet known how these performance measures translate into fitness.     

The molecular basis of speciation: from patterns to processes,rules to mechanisms

The empirical study of speciation has brought us closer to unlocking the origins of life’s vast diversity. By examining recently formed species, a number of general patterns, or rules, become apparent. Among fixed differences between species, sexual genes and traits are one of the most rapidly evolving and novel functional classes, and premating isolation often develops earlier than postmating isolation. Among interspecific hybrids, sterility evolves faster than inviability, the X-chromosome has a greater effect on incompatibilities than autosomes, and hybrid dysfunction affects the heterogametic sex more frequently than the homogametic sex (Haldane’s rule). Haldane’s rule, in particular, has played a major role in reviving interest in the genetics of speciation. However, the large genetic and reproductive differences between taxa and the multi-factorial nature of each rule have made it difficult to ascribe general mechanisms. Here, we review the extensive progress made since Darwin on understanding the origin of species. We revisit the rules of speciation, regarding them as landmarks as species evolve through time. We contrast these ‘rules’ of speciation to ‘mechanisms’ of speciation representing primary causal factors ranging across various levels of organization—from genic to chromosomal to organismal. To explain the rules, we propose a new ‘hierarchical faster-sex’ theory: the rapid evolution of sex and reproduction-related (SRR) genes (faster-SRR evolution), in combination with the preferential involvement of the X-chromosome (hemizygous X-effects) and sexually selected male traits (faster-male evolution). This unified theory explains a comprehensive set of speciation rules at both the prezyotic and postzygotic levels and also serves as a cohesive alternative to dominance, composite, and recent genomic conflict interpretations of Haldane’s rule.     

SPONTANEOUS MUTATIONS FOR LIFE-HISTORY CHARACTERS IN AN OBLIGATE PARTHENOGEN

By allowing mutations to accumulate spontaneously in different lines derived from a single female of an obligately parthenogenetic Daphnia, it has become possible to estimate the rate at which new genetic variance for life-history characters arises as well as to identify the average pleiotropic effects of mutant polygenes. The estimated polygenic mutation rates are quite compatible with those available for sexual organisms. The results are therefore in conflict with the hypothesis that parthenogens compensate for the loss of recombination by elevating the mutation rate. Based on these results, it is argued that the rate of phenotypic evolution may be enhanced as much as five-fold by sexuality. However, if dominance or epistatic gene interactions are of major importance, or if the sensitivity to environmental effects is reduced or the rate of polygenic mutation enhanced under asexuality, the full advantage of sex will not be attained and may even be reversed. Regardless of these conditions, it is clear that the mutational rate of production of polygenic variation is sufficient to allow significant rates of phenotypic evolution in purely asexual organisms.     

Vertebrate limb regeneration and the origin of limb stem cells

The existence of multipotent cells in the adult tissues and organs of those vertebrates that are capable of regeneration has been accepted for decades. Although studies of vertebrate limb regeneration have yet to identify many of the specific molecules involved in regeneration, numerous tissue grafting experiments and studies of cell lineage have contributed significantly to an understanding of the origin, activation, proliferation and cell-cell interactions of these progenitor cells. This has allowed the development of ideas about the regulation of pattern formation to restore the structure and function of lost tissues and organs. An understanding of the molecular mechanisms controlling these processes has lagged behind the dramatic advances achieved with other model organisms. However, given the intense, new research interest in stem cells over the past few years, there is good reason to be encouraged that insights about the biology of mammalian stem cells will accelerate progress in understanding the biology of regeneration in organisms that can regenerate. Advances in regeneration research will then feed back in terms of devising new strategies for therapies to induce regeneration in organisms such as humans that have traditionally been viewed as incapable of regeneration.     

No evidence for faster male hybrid sterility in population crosses of an intertidal copepod (Tigriopus californicus)

Two different forces are thought to contribute to the rapid accumulation of hybrid male sterility that has been observed in many inter-specific crosses, namely the faster male and the dominance theories. For male heterogametic taxa, both faster male and dominance would work in the same direction to cause the rapid evolution of male sterility; however, for taxa lacking differentiated sex chromosomes only the faster male theory would explain the rapid evolution of male hybrid sterility. It is currently unknown what causes the faster evolution of male sterility, but increased sexual selection on males and the sensitivity of genes involved in male reproduction are two hypotheses that could explain the observation. Here, patterns of hybrid sterility in crosses of genetically divergent copepod populations are examined to test potential mechanisms of faster male evolution. The study species, Tigriopus californicus, lacks differentiated, hemizygous sex chromosomes and appears to have low levels of divergence caused by sexual selection acting upon males. Hybrid sterility does not accumulate more rapidly in males than females in these crosses suggesting that in this taxon male reproductive genes are not inherently more prone to disruption in hybrids.     

Baroreceptor reflex control of heart rate in rats studied by induced and autogenic changes in arterial pressure

The function of the arterial baroreflex has traditionally been assessed by measurement of reflex changes in heart rate (HR) or sympathetic nerve activity resulting from experimenter-induced manipulation of arterial blood pressure (the Oxford method, also termed the pharmacological method). However, logistical and flexibility limitations of this technique have promoted the development of new methods for assessing baroreflex function such as the evaluation of changes in spontaneous arterial pressure and HR. Although this new spontaneous method has been validated in dogs and humans, it has not been rigorously tested in rats. In the present study, the method of correlating spontaneous changes in systolic blood pressure and HR was evaluated in resting, normotensive Sprague-Dawley rats. This technique was found to be neither reliable nor valid under the conditions employed in the present protocol. We also tested a variation of the spontaneous method that evaluates particular sequences of data during which arterial pressure and pulse interval are changing in the same direction for at least three consecutive heartbeats (the sequence method). The sequence method did not provide extra reliability or validity over the spontaneous method. We conclude that due to the restricted range of variability obtained by measuring spontaneous blood pressure fluctuations, the spontaneous and sequence techniques do not provide data that are comparable to the traditional method of assessing HR changes triggered by arterial blood pressure increases and decreases induced by vasoactive drugs. However, it is possible that surgical stress obscured the relationship between blood pressure and HR, and therefore additional studies are needed to determine whether the spontaneous and sequence methods can be applied to rats during different behavioral states.     

Sex Chromosomes and Male Functions: Where Do New Genes Go?

The position of a gene in the genome may have important consequences for its function. Therefore, when a new duplicate gene arises, its location may be critical in determining its fate. Our recent work in humans, mouse, and Drosophila provided a test by studying the patterns of duplication in sex chromosome evolution. We revealed a bias in the generation and recruitment of new gene copies involving the X chromosome that has been shaped largely by selection for male germline functions. The gene movement patterns we observed reflect an ongoing process as some of the new genes are very young while others were present before the divergence of humans and mouse. This suggests a continuing redistribution of male-related genes to achieve a more efficient allocation of male functions. This notion should be further tested in organisms employing other sex determination systems or in organisms differing in germline X chromosome inactivation. It is likely that the selective forces that were detected in these studies are also acting on other types of duplicate genes. As a result, future work elucidating sex chromosome differentiation by other mutational mechanisms will shed light on this important process.     

Male–Male Relationships in Lion-tailed Macaques (<Emphasis Type="Italic">Macaca silenus</Emphasis>) and Bonnet Macaques (<Emphasis Type="Italic">Macaca radiata</Emphasis>)

Socioecology suggests that female distribution in space is determined by the distribution of food resources and the male distribution is influenced by female distribution. Though studies have traditionally focused on females, males have received increasing attention in recent years. We compared male–male relationships in lion-tailed macaques and bonnet macaques. Because bonnet macaques have a high adult male:female sex ratio and are seasonal breeders whereas lion-tailed macaques have a low adult male:female sex ratio and are largely aseasonal breeders, we predicted that bonnet macaque males would be spatially and socially more tolerant of each other and would have less linear dominance relationships than lion-tailed macaques. We recorded male–male and male–female relationships in 1 group of wild macaques of each species via scan sampling and 1–0 sampling. The results revealed that lion-tailed macaque males largely remained at a distance from each other whereas bonnet macaque males remained in close proximity to one another. Lion-tailed macaque males were more agonistic toward each other whereas bonnet macaque males showed more affiliative interactions. The dominance hierarchy among lion-tailed macaque males was more linear than among bonnet macaque males. Our data support the hypothesis that the study of spatial structuring, temporality of interactions, and linearity of social relationships may contribute to a better understanding of macaque social systems.     

Disturbance and recovery of microbial community structure and function following Hurricane Frances

Disturbance and recovery influence microbial community structure and ecosystem functions in most natural environments. This study from a hypersaline Bahamian lagoon details the response of a benthic cyanobacterial mat to disturbance by Hurricane Frances, a category-4 storm. Clone libraries of cyanobacterial small subunit r-RNA genes and nitrogenase genes revealed significant shifts in cyanobacterial and diazotroph community composition following the hurricane. Post-hurricane clone libraries were dominated by sequences that had been rare in pre-hurricane communities. In spite of this dominance shift, re-colonizing mat communities performed nitrogen fixation and photosynthesis at rates within the normal range of variation measured in the mat at similar salinities. There was a tendency for nitrogen fixation rates from mats re-colonizing sites with hurricane-related sand deposition to be higher than those from mats re-colonizing sites without significant sand deposition. This suggests that the altered communities responded to a carbon : nitrogen imbalance that was particularly pronounced in areas subjected to disturbance by sand burial. The post-hurricane dominance of organisms that had been previously rare suggests that pre-hurricane diversity and functional redundancy contributed to the rapid recovery of ecosystem function in the post-disturbance environment.     

Dominance and reproductive success among nonhuman animals: A cross-species comparison

This paper updates and extends Dewsbury's (1982) review of the literature on dominance and reproductive success (RS). The findings from approximately 700 studies are included, over two thirds of which were unavailable to Dewsbury. In order to give a highly condensed and yet meaningful overview, the main findings are represented in four tables, one for male nonprimates, one for female nonprimates, one for male primates, and one for female primates. In the tables for males, findings are analyzed in terms of six different indicators of RS, and in the tables for females, in terms of eight RS indicators.Outside the primate order, evidence largely supported the hypothesis that high-ranking males enjoy greater RS than do subordinate males. For females, studies are more evenly divided between those supporting the hypothesis that high rank and RS are positively correlated and those indicating no significant rank-RS relationship. This may reflect both the lower saliency of hierarchical relationships among females, as well as the lower variability in RS among females, relative to males.Among primates, a complex picture has emerged, especially in the case of males. Much of the complexity appears due to the importance of age and seniority in affecting dominance rank. Also, in some primate species, female preferences for sex partners seem to have little to do with the male's dominance rank, at least at the time mating takes place. Nevertheless, the majority of studies suggest that high- to middle-ranking males have at least a slight lifetime reproductive advantage over the lowest ranking males.     

A sex difference in the context-sensitivity of dominance perceptions

Although dominance perceptions are thought to be important for effective social interaction, their primary function is unclear. One possibility is that they simply function to identify individuals who are capable of inflicting substantial physical harm, so that the perceiver can respond to them in ways that maximize their own physical safety. Another possibility is that they are more specialized, functioning primarily to facilitate effective direct (i.e., violent) intrasexual competition for mates, particularly among men. Here we used a priming paradigm to investigate these two possibilities. Facial cues of dominance were more salient to women after they had been primed with images of angry men, a manipulation known to activate particularly strong self-protection motivations, than after they had been primed with images of angry women or smiling individuals of either sex. By contrast, dominance cues were more salient to men after they had been primed with images of women than when they had been primed with images of men (regardless of the emotional expressions displayed), a manipulation previously shown to alter men's impressions of the sex ratio of the local population. Thus, men's dominance perceptions appear to be specialized for effective direct competition for mates, while women's dominance perceptions may function to maximize their physical safety more generally. Together, our results suggest that men's and women's dominance perceptions show different patterns of context-sensitivity and, potentially, shed new light on the routes through which violence and intrasexual competition have shaped dominance perceptions.     

Population differentiation in the beetle Tribolium castaneum. II. Haldane'S rule and incipient speciation

The heterogametic sex tends to be rare, absent, sterile, or deformed in F1 hybrid crosses between species, a pattern called Haldane's rule (HR). The introgression of single genes or chromosomal regions from one drosophilid species into the genetic background of another have shown that HR is most often associated with fixed genetic differences in inter-specific crosses. However, because such introgression studies have involved species diverged several hundred thousand generations from a common ancestor, it is not clear whether HR attends the speciation process or results from the accumulation of epistatically acting genes postspeciation. We report the first evidence for HR prior to speciation in crosses between two populations of the red flour beetle, Tribolium castaneum, collected 931 km apart in Colombia and Ecuador. In this cross, HR is manifested as an increase in the proportion of deformed males compared to females and the expression of HR is temperature dependent. Neither population, when crossed to a geographically distant population from Japan, exhibits HR at any rearing temperature. Using joint-scaling analysis and additional data from backcrosses and F2's, we find that the hybrid incompatibilities and the emergence of HR are concurrent processes involving interactions between X-linked and autosomal genes. However, we also find many examples of incompatibilities manifest by F2 and backcross hybrids but not by F1 hybrids and most incompatibilities are not sex different in their effects, even when they involve both X-autosomal interactions and genotype-by-environment interactions. We infer that incipient speciation in flour beetles can occur with or without HR and that significant hybrid incompatibilities result from the accumulation of epistatically acting gene differences between populations without differentially affecting the heterogametic sex in F1 hybrids. The temperature dependence of the incompatibilities supports the inference that genotype-by-environment interactions and adaptation to different environments contribute to the genetic divergence important to postzygotic reproductive isolation.     

High-resolution genome-wide dissection of the two rules of speciation in Drosophila

Postzygotic reproductive isolation is characterized by two striking empirical patterns. The first is Haldane's rule—the preferential inviability or sterility of species hybrids of the heterogametic (XY) sex. The second is the so-called large X effect—substitution of one species's X chromosome for another's has a disproportionately large effect on hybrid fitness compared to similar substitution of an autosome. Although the first rule has been well-established, the second rule remains controversial. Here, we dissect the genetic causes of these two rules using a genome-wide introgression analysis of Drosophila mauritiana chromosome segments in an otherwise D. sechellia genetic background. We find that recessive hybrid incompatibilities outnumber dominant ones and that hybrid male steriles outnumber all other types of incompatibility, consistent with the dominance and faster-male theories of Haldane's rule, respectively. We also find that, although X-linked and autosomal introgressions are of similar size, most X-linked introgressions cause hybrid male sterility (60%) whereas few autosomal introgressions do (18%). Our results thus confirm the large X effect and identify its proximate cause: incompatibilities causing hybrid male sterility have a higher density on the X chromosome than on the autosomes. We evaluate several hypotheses for the evolutionary cause of this excess of X-linked hybrid male sterility.     

A novel PCR‐based genetic marker shows that sex of offspring does not account for hatch‐order effects on growth,survival and dominance in Pūkeko Porphyrio melanotus melanotus

Intra‐brood competition can influence a variety of fitness‐related traits in birds. Previous research on the joint‐nesting Pūkeko Porphyrio melanotus melanotus, a New Zealand subspecies of Australasian Swamphen, showed that chicks that hatched earlier in a brood tended to grow faster, were more likely to survive and had higher dominance status as adults than later hatched nest‐mates. However, this finding could be due to changes in offspring sex ratio across hatch order (e.g. if males tend to hatch earlier), which was not previously examined because of methodological challenges associated with sexing nestling Pūkeko. Here, we report a useful PCR‐based genetic marker to determine the sex of Pūkeko. We then used new sex‐specific data to re‐examine patterns of offspring growth, survival and dominance. We found that the sex of offspring does not account for the hatching‐order patterns related to social dominance, growth or survival. Furthermore, changes in offspring sex ratio across hatching‐order were negligible and offspring sex ratios did not differ significantly between the primary female and secondary female broods (in joint‐clutch nests), or when comparing primary female and single female broods. We found no clear evidence for sex ratio bias according to hatching‐order and conclude that hatching‐order and not offspring sex explain patterns of growth, survivorship and adult dominance in Pūkeko.     

An integrated classification for polymorphism and sexual dimorphism in butterflies

In bisexual organisms, pattern polymorphism may affect both sexes equally (unimodal polymorphism), or be expressed differently in the two sexes (bimodal polymorphism). Bimodal species may or may not have one or more forms that are identical in both sexes (shared morphs), in addition to those pattern forms which only occur in a particular sex (sex-limited morphs). Sex-limited morphs may occur in the male sex only, the female sex only, or be found in both sexes. Bimodal species in which there are no shared morphs show complete sex-limitation of pattern (dualism), in contrast to those in which there are shared morphs, which may be said to exhibit partial sex-limitation. Sexual dimorphism is here divided into two categories, partial sexual dimorphism (where both similar and dissimilar prospective pairs coexist), and complete sexual dimorphism (where only dissimilar prospective pairs coexist). From these considerations a comprehensive classification of nine categories of phaneromorphic polymorphism is developed, including monomorphism as the limiting case. This classification is presented graphically for convenient reference and visualisation. Selected examples of each class as they occur in butterflies are given, for both mimetic and non-mimetic species. The necessity for such a classification as a tool in the study of the evolution of polymorphism, sexual dimorphism and mimicry in butterflies is briefly discussed. This classification should also prove relevant to polymorphism studies in all non-parthenogenetic, bisexually reproducing species of organisms.