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PubMed2005

Cryptic speciation and host-race formation in a purportedly generalist tumbling flower beetle.

Host-race formation remains controversial as a source of herbivorous insect diversity, and examples of host races are still fairly scarce. In this study, analysis of five enzyme loci in the ostensibly generalist tumbling flower beetle Mordellistena convicta (Coleoptera: Mordellidae) revealed hidden host-plant and plant-organ related genetic differentiation. Mordellistena convicta turned out to be a complex of cryptomorphic species, each with fewer hosts than the nominal species. These cryptic species, in turn, were divided into taxa that showed host-race characteristics: samples from different host plants and organs exhibited (1) genetic indications of partial reproductive isolation, (2) differences in size and emergence timing that suggested divergent host-related selection, and (3) among-host selective differences in mortality from parasitoids. Host-race formation in M. convicta, which has a somewhat different life history from the well-studied host races, enlarges the group of insects considered likely to undergo this process. The widespread sympatry of the M. convicta species complex, along with its spectrum of host-correlated genetic differentiation, suggests that these host specialist taxa developed in sympatry.

Adaptation, Biological↗
PubMed2006

Gene regulation divergence is a major contributor to the evolution of Dobzhansky-Muller incompatibilities between species of Drosophila.

The Dobzhansky-Muller model denotes incompatible gene interactions between diverging populations/species and is recognized as the basis of postzygotic reproductive isolation. Little is known about the molecular nature of such gene interactions. We have carried out comparative gene expression analyses in the testes of 3 closely related species of the Drosophila melanogaster subgroup and their hybrids (all of which are sterile). We show that in hybrids 1) a higher proportion of male-biased genes (i.e., genes with a higher level of expression in males) are underexpressed (or not expressed) compared with non-sex-biased genes, 2) the majority of the underexpressed genes appear to be under stabilizing selection by virtue of showing similar levels of expression in the parental species, and only a small proportion of genes show signs of directional selection, 3) very few of the misexpressed genes are shared between species pairs, suggesting that there may not be a "common" set of "speciation genes," and 4) expression of non-testes-specific genes is observed in the testes of interspecific hybrids, and the number of such genes is positively correlated with divergence time. These results suggest that gene regulation divergence of sex- and reproduction-related genes is a major contributor to the evolution of Dobzhansky-Muller incompatibilities between species of Drosophila.

Animals↗
PubMed2000

Characterization of defects in adult germline development and oogenesis of sterile and rescued female hybrids in crosses between Drosophila simulans and Drosophila melanogaster.

Crosses between Drosophila melanogaster and D. simulans normally result in progeny that are either inviable or sterile. Recent discovery of strains that rescue these inviability and sterility phenotypes has made it possible to study the developmental basis of reproductive isolation between these two species in greater detail. By producing both rescued and unrescued hybrids and examining the protein product staining patterns of genes known to be involved in early germline development and gametogenesis, we have found that in crosses between D. simulans and D. melanogaster, hybrid female sterility results from the improper control of primordial germline proliferation, germline stem cell maintenance, and cystoblast formation and differentiation during early oogenesis. Rescued hybrid females are fertile, yet they generally have lower amounts of adult germline from the outset and show a premature degeneration of adult germline cells with age. In addition, older rescued hybrid females also exhibit mutant egg phenotypes associated with defects in dorso-ventral patterning which may result from the improper partitioning of cytoplasmic factors during early oogenesis that could stem from the early defect. Although a variety of germline and oogenic defects are described for the hybrid females, all of them can potentially result from the same underlying primary defect. Hybrid males from these same crosses, on the other hand, have no detectable germline in adult reproductive tissues, even when hybrid sterility rescue strains are used, indicating that male sterility and female sterility stem from distinctly different developmental defects.

Animals↗
PubMed2006

Site-specific genetic divergence in parallel hybrid zones suggests nonallopatric evolution of reproductive barriers.

The evolution of reproductive isolation in the presence of gene flow is supported by theoretical models but rarely by data. Empirical support might be gained from studies of parallel hybrid zones between interbreeding taxa. We analysed gene flow over two hybrid zones separating ecotypes of Littorina saxatilis to test the expectation that neutral genetic markers will show site-specific differences if barriers have evolved in situ. Distinct ecotypes found in contrasting shore habitats are separated by divergent selection and poor dispersal, but hybrid zones appear between them. Swedish islands formed by postglacial uplift 5000 years ago provide opportunities to assess genetic structure in a recently evolved system. Each island houses a discrete population containing subpopulations of different ecotypes. Hybrid zones between ecotypes may be a product of ecological divergence occurring on each island or a consequence of secondary overlap of ecotypes of allopatric origin that have spread among the islands. We used six microsatellite loci to assess gene flow and genetic profiles of hybrid zones on two islands. We found reduced gene flow over both hybrid zones, indicating the presence of local reproductive barriers between ecotypes. Nevertheless, subpopulations of different ecotypes from the same island were genetically more similar to each other than were subpopulations of the same ecotype from different islands. Moreover, neutral genetic traits separating the two ecotypes across hybrid zones were site-specific. This supports a scenario of in situ origin of ecotypes by ecological divergence and nonallopatric evolution of reproductive barriers.

Animals↗
PubMed2000

Evolution of poecilogony and the biogeography of North American populations of the polychaete Streblospio.

Invertebrate interspecific developmental patterns can be highly variable and, taxonomically, are considered only weakly constrained. Intraspecifically, some invertebrate species possess multiple developmental modes-a condition known as poecilogony. Closer examination of most putative poecilogenous species, however, has not supported poecilogony, but rather has uncovered hidden or cryptic species. The polychaete Streblospio benedicti is a well-known, poecilogenous species found along the coast of North America. We collected mitochondrial cytochrome subunit I DNA sequence data from 88 individuals taken from 11 locations along the Atlantic, Gulf, and Pacific Coasts of the United States to provide a phylogenetic framework from which to interpret intraspecific variation in larval life history and brooding structure morphology in this species. Our results are consistent with a recent revision of the species into two separate species: S. benedicti, a pouched brooding form distributed along the Atlantic and Pacific Coasts, and S. gynobranchiata, a branchiate brooding form in the Gulf of Mexico. Contrary to the redescription, S. benedicti is paraphyletic because the pouched brooding population in Vero Beach, Florida shows strong genetic affinity with Gulf of Mexico populations (S. gynobranchiata). However, S. benedicti is a true poecilogenous species, with both lecithotrophic and planktotrophic individuals possessing identical mitochondrial DNA haplotypes. Crossbreeding experiments further support the molecular phylogeny with reproductive isolation demonstrated between, but not within, the major phylogenetic clades consistent with the previously described species. The genetic break near Vero Beach, Florida, corresponds to a well-known phylogeographic boundary, but the estimated time of separation for the Streblospio spp., approximately 10 million years before present, predates all other known phylogeographic subdivisions in this area. This suggests that biogeographic sundering in this region is a recurrent event. Divergence times within the major Streblospio spp. clades are recent and indicate that changes in larval life history as well as brooding structure morphology are highly plastic and can evolve rapidly.

Animals↗
PubMed2005

Variable assortative mating in replicate mating trials using Drosophila melanogaster populations derived from contrasting opposing slopes of 'Evolution Canyon', Israel.

Significant assortative mating in laboratory studies has been previously shown between two populations of Drosophila melanogaster collected from micro-climactically contrasting and opposing slopes of 'Evolution Canyon' (Lower Nahal Oren, Israel; Korol et al., 2000). Coupled with evidence that the two populations are adapted to their respective environments, this has been suggested as a rare example of ongoing behaviourally mediated speciation occurring in the face of gene flow. Reproductive isolation between these populations, however, has never been confirmed by replicate experiments in an independent laboratory. For this reason, we tested recent collections of these populations for premating isolation in both the original (Haifa) and a new (Burnaby) laboratory under a variety of experimental protocols. Although non-random mating was found in the majority of trials conducted in Haifa, we were unable to replicate these strong results in Burnaby. Most notably, we failed to detect assortative mating in four separate double choice experiments. Significant non-random mating was detected, however, in three of six single choice experiments in Burnaby, suggesting that the populations are behaviourally differentiated in some manner. Why nonrandom mating was weaker in Burnaby than Haifa is not understood, but suggests that assortative mating may be sensitive to unknown environmental factors.

Animals↗
PubMed2001

Cross-fertility in two tropical tree species: evidence of inbreeding depression within populations and genetic divergence among populations.

Knowing the spatial patterns of cross-fertility in natural plant populations yields key insight into biparental inbreeding depression, isolation by distance, and, ultimately, speciation. Three adults each of two tropical tree species (Syzygium rubicundum and Shorea cordifolia) were each crossed with five conspecific pollen donors ranging from self to trees occurring in separate forest reserves (12 and 35 km distance for S. rubicundum and Sh. cordifolia, respectively). Cross-fertility was estimated as fruit set, seed germination, and seedling survivorship and height at 1 yr. Means of most cross-fertility measures increased steadily with outcrossing distance, peaking at 1-2 km for S. rubicundum and 1-10 km for Sh. cordifolia, and then declining at the between-forest crosses. However, seed germination and seedling height for Sh. cordifolia suggested hybrid vigor in between-forest crosses. The mean fitness cost of nearest-neighbor mating relative to crossing with more distant neighbors was 45% for S. rubicundum and 0% for Sh. cordifolia. The mean fitness cost of between-forest crosses was 52% and 70% for the two species. Crossing effects on fitness diminished between the stages of fruit set and 1-yr-old seedlings. Results indicate a strong potential for inbreeding depression within forest tree populations and partial reproductive isolation among forests in Sri Lanka's wet zone.

Journal Article↗
PubMed1999

Two levels of information in DNA: relationship of Romanes' "intrinsic" variability of the reproductive system, and Bateson's "residue" to the species-dependent component of the base composition, (C+G)%.

In 1886 Charles Darwin's research associate George Romanes published a paper entitled "Physiological Selection: An Additional Suggestion on the Origin of Species". This was criticized by his Victorian contemporaries and largely ignored by those who followed. However, the recent recognition of two levels of information in DNA suggests that Romanes had solved the major problems with Darwin's theory. It was apparent from the outset that the form of reproductive isolation likely to apply most generally to initial species divergence (hybrid sterility), would depend on differences, not in "primary" information ("genic"), but in "secondary" information ("chromosomal"). This viewpoint, further elaborated by Bateson & Saunders (1902), White (1978), and King (1993), is criticized by the genic school (Coyne & Orr, 1998) because it requires visible differences between chromosomes, and appears not to explain Haldane's rule. However, chromosomal differentiation with respect to the species-dependent component of base composition [(C+G)%; Forsdyke, 1996] appears to resolve these problems. Because it explained so much, it was easy to believe that the genic viewpoint explained everything. Romanes and Bateson thought otherwise. We are only just beginning to recognize what they were trying to tell us.

Animals↗
PubMed2006

Macroevolutionary data suggest a role for reinforcement in pollination system shifts.

Reproductive isolation can evolve either as a by-product of divergent selection or through reinforcement. We used the Cape flora of South Africa, known for its high level of pollination specialization, as a model system to test the potential role of shifts in pollination system in the speciation process. Comparative analysis of 41 sister-species pairs (representing Geraniaceae, Iridaceae, and Orchidaceae) for which complete pollinator, edaphic, and distribution data are available showed that for sister species with overlapping distribution ranges, pollination system shifts are significantly associated with edaphic shifts. In contrast, there is no significant association between pollination system shifts and edaphic shifts for allopatric sister species. These results are interpreted as evidence for reinforcement.

Biological Evolution↗
PubMed2004

Life-history divergence in Chinook salmon: historic contingency and parallel evolution.

By jointly considering patterns of genetic and life-history diversity in over 100 populations of Chinook salmon from California to British Columbia, we demonstrate the importance of two different mechanisms for life-history evolution. Mapping adult run timing (the life-history trait most commonly used to characterize salmon populations) onto a tree based on the genetic data shows that the same run-time phenotypes exist in many different genetic lineages. In a hierarchical gene diversity analysis, differences among major geographic and ecological provinces explained the majority (62%) of the overall G(ST), whereas run-time differences explained only 10%. Collectively, these results indicate that run-timing diversity has developed independently by a process of parallel evolution in many different coastal areas. However, genetic differences between coastal populations with different run timing from the same basin are very modest (G(ST) < 0.02), indicating that evolutionary divergence of this trait linked to reproductive isolation has not led to parallel speciation, probably because of ongoing gene flow. A strikingly different pattern is seen in the interior Columbia River Basin, where run timing and other correlated life-history traits map cleanly onto two divergent genetic lineages (G(ST) approximately 0.15), indicating that some patterns of life-history diversity have a much older origin. Indeed, genetic data indicate that in the interior Columbia Basin, the two divergent lineages behave essentially as separate biological species, showing little evidence of genetic contact in spite of the fact that they comigrate through large areas of the river and ocean and in some locations spawn in nearly adjacent areas.

Animal Migration↗
PubMed2006

Evolutionary conflicts of interest between males and females.

Sexual conflict arises from differences in the evolutionary interests of males and females and can occur over traits related to courtship, mating and fertilisation through to parental investment. Theory shows that sexual conflict can lead to sexually antagonistic coevolution (SAC), where adaptation in one sex can lead to counter-adaptation in the other. Thus, sexual conflict can lead to evolutionary change within species. In addition, SAC can--through its effects on traits related to the probability of mating and of zygote formation--potentially lead to reproductive isolation. In this review, I discuss that, although sexual conflict is ubiquitous, the actual expression of sexual conflict leading to SAC is less frequent. The balance between the benefits and costs of the manipulation of one sex by the other, and the availability of mechanisms by which conflict is expressed, determine whether actual sexual conflict is likely to occur. New insights address the relationship between sexual conflict and conflict resolution, adaptation, sexual selection and fitness. I suggest that it will be useful to examine systematically the parallels and contrasts between sexual and other evolutionary conflicts. Understanding why some traits, but not others, are subject to evolutionary change by SAC will require data on the mechanisms of the traits involved and on the relative benefits and costs of manipulation and resistance to manipulation.

Animals↗
PubMed2002

Speciation despite gene flow when developmental pathways evolve.

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.

Animals↗
PubMed1999

Epigenetic inheritance, genetic assimilation and speciation.

Epigenetic inheritance systems enable the environmentally induced phenotypes to be transmitted between generations. Jablonka and Lamb (1991, 1995) proposed that these systems have a substantial role during speciation. They argued that divergence of isolated populations may be first triggered by the accumulation of (heritable) phenotypic differences that are later followed and strengthened by genetic changes. The plausibility of this idea is examined in this paper. At first, we discuss the "exploratory" behaviour of an epigenetic inheritance system on a one peak adaptive landscape. If a quantitative trait is far from the optimum, then it is advantageous to induce heritable phenotypic variation. Conversely, if the genotypes get closer to the peak, it is more favorable to canalize the phenotypic expression of the character. This process would lead to genetic assimilation. Next we show that the divergence of heritable epigenetic marks acts to reduce or to eliminate the genetic barrier between two adaptive peaks. Therefore, an epigenetic inheritance system can increase the probability of transition from one adaptive state to another. Peak shift might be initiated by (i) slight changes in the inducing environment or by (ii) genetic drift of the genes controlling epigenetic variability. Remarkably, drift-induced transition is facilitated even if phenotypic variation is not heritable. A corollary of our thesis is that evolution can proceed through suboptimal phenotypic states, without passing through a deep adaptive valley of the genotype. We also consider the consequences of this finding on the dynamics and mode of reproductive isolation.

Animals↗
PubMed2001

Molecular evolution of the ocnus and janus genes in the Drosophila melanogaster species subgroup.

Genes involved in male fertility are potential targets for sexual selection, and their evolution may play a role in reproductive isolation and speciation. Here we describe a new Drosophila melanogaster gene, ocnus (ocn), that encodes a protein abundant in testes nuclear extracts. RT-PCR indicates that ocn transcription is limited to males and is specific to testes. ocn shares homology with another testis-specific gene, janusB (janB), and is located just distal to janB on chromosome 3. The two genes also share homology with the adjacent janusA (janA) gene, suggesting that multiple duplication events have occurred within this region of the genome. We cloned and sequenced these three genes from species of the D. melanogaster species subgroup. Phylogenetic analysis based on protein-encoding sequences predicts a duplication pattern of janA --> janA janB --> janA janB ocn, with the latter event occurring after the divergence of the D. melanogaster and Drosophila obscura species groups. We found significant heterogeneity in the rates of evolution among the three genes within the D. melanogaster species subgroup as measured by the ratio of nonsynonymous to synonymous substitutions, suggesting that diversification of gene function followed each duplication event and that each gene evolved under different selective constraints. All three genes showed faster rates of evolution than genes encoding proteins with metabolic function. These results are consistent with previous studies that have detected an increased rate of evolution in genes with reproductive function.

Animals↗
PubMed2003

Engineering evolution to study speciation in yeasts.

The Saccharomyces 'sensu stricto' yeasts are a group of species that will mate with one another, but interspecific pairings produce sterile hybrids. A retrospective analysis of their genomes revealed that translocations between the chromosomes of these species do not correlate with the group's sequence-based phylogeny (that is, translocations do not drive the process of speciation). However, that analysis was unable to infer what contribution such rearrangements make to reproductive isolation between these organisms. Here, we report experiments that take an interventionist, rather than a retrospective approach to studying speciation, by reconfiguring the Saccharomyces cerevisiae genome so that it is collinear with that of Saccharomyces mikatae. We demonstrate that this imposed genomic collinearity allows the generation of interspecific hybrids that produce a large proportion of spores that are viable, but extensively aneuploid. We obtained similar results in crosses between wild-type S. cerevisiae and the naturally collinear species Saccharomyces paradoxus, but not with non-collinear crosses. This controlled comparison of the effect of chromosomal translocation on species barriers suggests a mechanism for the generation of redundancy in the S. cerevisiae genome.

Aneuploidy↗
PubMed2004

A test of the chromosomal rearrangement model of speciation in Drosophila pseudoobscura.

Recent studies suggest that chromosomal rearrangements play a significant role in speciation by preventing recombination and maintaining species persistence despite interspecies gene flow. Factors conferring adaptation or reproductive isolation are maintained in rearranged regions in the face of hybridization, while such factors are eliminated from collinear regions. As a direct test of this rearrangement model, we evaluated the genetic basis of hybrid male sterility in a sympatric species pair, Drosophila pseudoobscura pseudoobscura and D. persimilis, and an allopatric species pair, D. pseudoobscura bogotana and D. persimilis. Our results are consistent with the proposed model: virtually all of the sterility factors in the former pair are associated with three inverted regions, whereas sterility factors are present in the collinear regions in the latter pair. These findings indicate recombination and selection may have eliminated sterility factors outside the inverted regions between D. p. pseudoobscura and D. persimilis, suggesting chromosomal rearrangements may facilitate species persistence despite hybridization.

Animals↗
PubMed2004

Postmating sexual selection: allopatric evolution of sperm competition mechanisms and genital morphology in calopterygid damselflies (Insecta: Odonata).

Postmating sexual selection theory predicts that in allopatry reproductive traits diverge rapidly and that the resulting differentiation in these traits may lead to restrictions to gene flow between populations and, eventually, reproductive isolation. In this paper we explore the potential for this premise in a group of damselflies of the family Calopterygidae, in which postmating sexual mechanisms are especially well understood. Particularly, we tested if in allopatric populations the sperm competition mechanisms and genitalic traits involved in these mechanisms have indeed diverged as sexual selection theory predicts. We did so in two different steps. First, we compared the sperm competition mechanisms of two allopatric populations of Calopteryx haemorrhoidalis (one Italian population studied here and one Spanish population previously studied). Our results indicate that in both populations males are able to displace spermathecal sperm, but the mechanism used for sperm removal between both populations is strikingly different. In the Spanish population males seem to empty the spermathecae by stimulating females, whereas in the Italian population males physically remove sperm from the spermathecae. Both populations also exhibit differences in genital morphometry that explain the use of different mechanisms: the male lateral processes are narrower than the spermathecal ducts in the Italian population, which is the reverse in the Spanish population. The estimated degree of phenotypic differentiation between these populations based on the genitalic traits involved in sperm removal was much greater than the differentiation based on a set of other seven morphological variables, suggesting that strong directional postmating sexual selection is indeed the main evolutionary force behind the reproductive differentiation between the studied populations. In a second step, we examined if a similar pattern in genital morphometry emerge in allopatric populations of this and other three species of the same family (Calopteryx splendens, C. virgo and Hetaerina cruentata). Our results suggest that there is geographic variation in the sperm competition mechanisms in all four studied species. Furthermore, genitalic morphology was significantly divergent between populations within species even when different populations were using the same copulatory mechanism. These results can be explained by probable local coadaptation processes that have given rise to an ability or inability to reach and displace spermathecal sperm in different populations. This set of results provides the first direct evidence of intraspecific evolution of genitalic traits shaped by postmating sexual selection.

Animals↗
PubMed2014

Inter-genomic sexual conflict drives antagonistic coevolution in harvester ants.

The reproductive interests of males and females are not always aligned, leading to sexual conflict over parental investment, rate of reproduction and mate choice. Traits that increase the genetic interests of one sex often occur at the expense of the other, selecting for counter-adaptations leading to antagonistic coevolution. Reproductive conflict is not limited to intraspecific interactions; interspecific hybridization can produce pronounced sexual conflict between males and females of different species, but it is unclear whether such conflict can drive sexually antagonistic coevolution between reproductively isolated genomes. We tested for hybridization-driven sexually antagonistic adaptations in queens and males of the socially hybridogenetic 'J' lineages of Pogonomyrmex harvester ants, whose mating system promotes hybridization in queens but selects against it in males. We conducted no-choice mating assays to compare patterns of mating behaviour and sperm transfer between inter- and intra-lineage pairings. There was no evidence for mate discrimination on the basis of pair type, and the total quantity of sperm transferred did not differ between intra- and inter-lineage pairs; however, further dissection of the sperm transfer process into distinct mechanistic components revealed significant, and opposing, cryptic manipulation of copulatory investment by both sexes. Males of both lineages increased their rate of sperm transfer to high-fitness intra-lineage mates, with a stronger response in the rarer lineage for whom mating mistakes are the most likely. By contrast, the total duration of copulation for intra-lineage mating pairs was significantly shorter than for inter-lineage crosses, suggesting that queens respond to prevent excessive sperm loading by prematurely terminating copulation. These findings demonstrate that sexual conflict can lead to antagonistic coevolution in both intra-genomic and inter-genomic contexts. Indeed, the resolution of sexual conflict may be a key determinant of the long-term evolutionary potential of host-dependent reproductive strategies, counteracting the inherent instabilities arising from such systems.

Animals↗