Norman A. Johnson

Haldane's rule and its legacy: Why are there so many sterile males?

A general pattern of animal hybridization, known as Haldanes rule, is that the XY (ZW) sex is more severely affected in its viability or fertility than the XX (ZZ) sex. Recent evidence suggests that three different forces have shaped this pattern: (1) the X chromosome and autosomes are in greater disharmony in the XY sex; (2) evolution of hybrid male sterility is greatly accelerated, at least in species with XY males; and (3) maternal-zygotic incompatibility preferentially affects the viability of the XX sex. In species with XY males, the rapid evolution toward hybrid male sterility may be responsible for the bulk of observations pertaining to Haldanes rule. One interesting and testable hypothesis is that sexual selection drives this rapid evolution.

PATTERNS OF POSTZYGOTIC ISOLATION IN FROGS

From literature data on 116 taxa crosses involving 46 species of frogs, we found a positive correlation between degree of divergence (measured as Neis genetic distance, D) and degree of postzygotic isolation. In anurans, hybrid sterility appears to evolve more quickly than inviability, which is consistent with the conclusions of other studies that involved Drosophila species. The lower threshold of D = 0.30 for evolution of hybrid inviability that we found is similar to that observed for Drosophila. This consistency suggests that there may be a general pattern in the acquisition of reproductive isolation in animals.

Hybrid incompatibility genes: remnants of a genomic battlefield?

Hybrid incompatibility (including sterility, lethality, and less extreme negative effects) interests evolutionary biologists because of its role in speciation as a reproductive isolating barrier. It also has unusual genetic properties, being mainly due to interactions between at least two genes. Recent studies have identified some of the interacting genes that underlie hybrid incompatibility. These genes represent a wide array of functions, including those involved in oxidative respiration, nuclear trafficking, DNA-binding, and plant defense. Accumulating evidence suggests genomic conflict frequently drives the divergence causing incompatibilities in hybrids. The evidence bearing on this genomic conflict hypothesis is assessed and ways to test it conclusively are suggested.

Postcopulatory, prezygotic isolation in flour beetles.

We report the existence of postmating but prezygotic reproductive isolation within flour beetles of the genus Tribolium. Specifically, when a female of either T. castaneum or T. freemani is paired simultaneously with both a conspecific and a heterospecific male, virtually all of the offspring are sired by the conspecific male. In contrast, when a female of either species is paired only with a heterospecific male, she produces near normal numbers of offspring. Mate choice experiments rule out the possibility that premating reproductive isolation accounts for this phenomenon. A number of different mechanisms could explain this phenomenon of postmating but prezygotic reproductive isolation.

SPECIATION DESPITE GENE FLOW WHEN DEVELOPMENTAL PATHWAYS EVOLVE

Abstract.— Evolutionary biologists assume that species formation requires a drastic reduction in gene exchange between populations, but the rate sufficient to prevent speciation is unknown. To study speciation, we use a new class of population genetic models that incorporate simple developmental genetic rules, likely present in all organisms, to construct the phenotype. When we allow replicate populations to evolve in parallel to a new, shared optimal phenotype, often their hybrids acquire poorly regulated phenotypes: Dobzhansky‐Muller incompatibilities arise and postzygotic reproductive isolation evolves. Here we show that, although gene exchange does inhibit this process, it is the proportion of migrants exchanged (m) rather than the number of migrants (Nm) that is critical, and rates as high as 16 individuals exchanged per generation still permit the evolution of postzygotic isolation. Stronger directional selection counters the inhibitory effect of gene flow, increasing the speciation probability. We see similar results when populations in a standard two‐locus, two‐allele Dobzhansky‐Muller model are subject to simultaneous directional selection and gene flow. However, in developmental pathway models with more than two loci, gene flow is more able to impede speciation. Genetic incompatibilities arise as frequent by‐products of adaptive evolution of traits determined by regulatory pathways, something that does not occur when phenotypes are modeled using the standard, additive genetic framework. Development therefore not only constrains the microevolutionary process, it also facilitates the interactions among genes and gene products that make speciation more likely–even in the face of strong gene flow.

Evolution of branched regulatory genetic pathways: directional selection on pleiotropic loci accelerates developmental system drift

Developmental systems are regulated by a web of interacting loci. One common and useful approach in studying the evolution of development is to focus on classes of interacting elements within these systems. Here, we use individual-based simulations to study the evolution of traits controlled by branched developmental pathways involving three loci, where one locus regulates two different traits. We examined the system under a variety of selective regimes. In the case where one branch was under stabilizing selection and the other under directional selection, we observed “developmental system drift”: the trait under stabilizing selection showed little phenotypic change even though the loci underlying that trait showed considerable evolutionary divergence. This occurs because the pleiotropic locus responds to directional selection and compensatory mutants are then favored in the pathway under stabilizing selection. Though developmental system drift may be caused by other mechanisms, it seems likely that it is accelerated by the same underlying genetic mechanism as that producing the Dobzhansky–Muller incompatibilities that lead to speciation in both linear and branched pathways. We also discuss predictions of our model for developmental system drift and how different selective regimes affect probabilities of speciation in the branched pathway system.

Reproductive isolation between two species of flour beetles, Tribolium castaneum and T. freemani: variation within and among geographical populations of T. castaneum.

Tribolium castaneum and T. freemani produce sterile hybrid progeny in reciprocal crosses. The reciprocal crosses differ significantly in the mean numbers of progeny, progeny sex ratios, hybrid male body size and male antennal and leg morphologies. These results suggest an effect of either the X chromosome or the cytoplasm on characteristics of F1 hybrids. In contrast, large X chromosome effects on morphological traits are not usually oberved in interspecific crosses among drosophilid flies. We also report large, significant differences in progeny numbers, body mass and degree of female bias in sex ratio between different geographic strains of T. castaneum when mated in reciprocal crosses with T. freemani. Sex ratio bias also varies significantly among matings within geographic strains of T. castaneum. When T. castaneum males are mated with T. freemani females, but not in the reciprocal cross, the F1 sex ratio is female biased, uncorrelated with family size and ranges from 57.14 per cent to 72.23 per cent female, depending on the geographic strain of the T. castaneum male.

Toward a new synthesis: Population genetics and evolutionary developmental biology

Despite the recent synthesis of developmental genetics and evolutionary biology, current theories of adaptation are still strictly phenomenological and do not yet consider the implications of how phenotypes are constructed from genotypes. Given the ubiquity of regulatory genetic pathways in developmental processes, we contend that study of the population genetics of these pathways should become a major research program. We discuss the role divergence in regulatory developmental genetic pathways may play in speciation, focusing on our theoretical and computational investigations. We also discuss the population genetics of molecular co-option, arguing that mutations of large effect are not needed for co-option. We offer a prospectus for future research, arguing for a new synthesis of the population genetics of development.

TEMPERATURE EFFECTS AND GENOTYPE-BY-ENVIRONMENT INTERACTIONS IN HYBRIDS: HALDANE'S RULE IN FLOUR BEETLES

When males of the flour beetle, Tribolium castaneum, are crossed to females of its close relative T. freemani, the sex ratio of the hybrids is female biased, owing in part to hybrid male mortality. Morphological abnormalities are also frequent in the surviving hybrid males, but not in the hybrid females. The finding that the heterogametic sex (male) is more adversely affected in interspecific crosses than the homogametic sex is consistent with Haldanes rule, which predicts that hybrid dysfunction should emerge as an indirect byproduct of divergent adaptation to differing environments. If so, environmental effects and genotype‐by‐environment interactions (GEI) should characterize the expression of Haldanes rule and interspecific hybrid traits in general. We used two wild‐collected populations of T. castaneum (from Infantes, Spain, and Madagascar) to investigate the effects of environmental variation on the expression of Haldanes rule. Males from each population were mated to several T. freemani females and the half‐sibling hybrid progenies were reared across a series of temperature regimes. For both populations, we found that hybrids raised at higher temperatures exhibited a more extreme expression of Haldanes rule: The hybrid sex ratios were more biased toward females and hybrid males had a much higher incidence of morphological abnormalities. The average response to temperature, the norm of reaction for Haldanes rule, varied between the two populations, and we found considerable and significant GEI for both hybrid traits within both populations. The evolutionary implications of these findings are discussed in the context of speciation arising as an indirect effect of local adaptation.

Postcopulatory, prezygotic isolation: intraspecific and interspecific sperm precedence in Tribolium spp., flour beetles

We investigated intraspecific and interspecific patterns of paternity in Tribolium castaneum, the flour beetle, by mating females either to pairs of conspecific males or to one conspecific and one heterospecific male of the closely related species, T. freemani. Females of both species store sperm in the spermatheca after copulation and postcopulatory, prezygotic reproductive isolation has been reported between this pair of species. When conspecific males of contrasting genotype were mated simultaneously to T. castaneum females, we observed extremely high levels of variation among females in the pattern of sperm precedence as shown by the offspring genotypes. In contrast, T. castaneum females mated simultaneously to a conspecific and a heterospecific male produced over 99 per cent conspecific progeny. When conspecific males were mated sequentially to T. castaneum females, within 3-7 days, all offspring were sired by the second male. In contrast, when a conspecific male was replaced with a T. freemani male, most females continued to produce only first-male, conspecific offspring for the next 10 days. When a heterospecific male was replaced with a conspecific male, T. castaneum females changed from producing hybrid to conspecific offspring within 3 days. We discuss the evolutionary implications of these findings.