Article

Genealogical Discordance and Patterns of Introgression and Selection Across a Cricket Hybrid Zone

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Abstract

In recently diverged species, ancestral polymorphism and introgression can cause incongruence between gene and species trees. In the face of hybridization, few genomic regions may exhibit reciprocal monophyly, and these regions, usually evolving rapidly under selection, may be important for the maintenance of species boundaries. In animals with internal fertilization, genes encoding seminal protein are candidate barrier genes. Recently diverged hybridizing species such as the field crickets Gryllus firmus and G. pennsylvanicus, offer excellent opportunities to investigate the origins of barriers to gene exchange. These recently diverged species form a well-characterized hybrid zone, and share ancestral polymorphisms across the genome. We analyzed DNA sequence divergence for seminal protein loci, housekeeping loci, and mtDNA, using a combination of analytical approaches and extensive sampling across both species and the hybrid zone. We report discordant genealogical patterns and differential introgression rates across the genome. The most dramatic outliers, showing near-zero introgression and more structured species trees, are also the only two seminal protein loci under selection. These are candidate barrier genes with possible reproductive functions. We also use genealogical data to examine the demographic history of the field crickets and the current structure of the hybrid zone.

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... This well-characterized hybrid zone is maintained by multiple barriers to gene exchange. Some barriers involve adaptation to different environments (temporal isolation: Harrison 1985; habitat association: Rand & Harrison 1989a; Ross & Harrison 2006; Larson et al. 2013b), whereas other barriers reflect differences in behaviour (mate choice: Maroja et al. 2009b) and sperm–egg interactions ( Larson et al. 2012b). There is no evidence for postzygotic barriers; hybrid offspring between the two species are viable, fertile and able to produce F2 offspring and backcross to the parental species. ...
... The field crickets diverged approximately 200,000 years ago (Willett et al. 1997; Maroja et al. 2009a) and hybridize in a zone composed of interspersed parental and mixed populations distributed along the eastern edge of the Appalachian mountains (). Multiple prezygotic barriers limit gene exchange between species, including habitat isolation ( Harrison and Bogdanowicz 1997; Larson et al. 2013 ), positive assortative mating (Maroja et al. 2009b), and asymmetrical postmating prezygotic barriers (). Crosses between G. firmus females and G. pennsylvanicus males have reduced egg laying (Maroja et al. 2009b; Larson et al. 2012a), and sperm do not successfully fuse with eggs (Larson et al. 2012b). ...
... Multiple prezygotic barriers limit gene exchange between species, including habitat isolation ( Harrison and Bogdanowicz 1997; Larson et al. 2013 ), positive assortative mating (Maroja et al. 2009b), and asymmetrical postmating prezygotic barriers (). Crosses between G. firmus females and G. pennsylvanicus males have reduced egg laying (Maroja et al. 2009b; Larson et al. 2012a), and sperm do not successfully fuse with eggs (Larson et al. 2012b). In contrast, the reciprocal cross (G. ...
Article
Hybrid zones are regions where individuals from genetically differentiated populations meet and mate, resulting in at least some offspring of mixed ancestry. Patterns of gene flow (introgression) in hybrid zones vary across the genome, allowing assessment of the role of individual genes or genome regions in reproductive isolation. Here, we document patterns of introgression between two recently diverged species of field crickets. We sampled at a very fine spatial scale and genotyped crickets for 110 highly differentiated single nucleotide polymorphisms (SNPs) identified through transcriptome scans. Using both genomic and geographic cline analysis, we document remarkably abrupt transitions (<100 m) in allele frequencies for 50 loci, despite high levels of gene flow at other loci. These are among the steepest clines documented for any hybridizing taxa. Furthermore, the cricket hybrid zone provides one of the clearest examples of the semi-permeability of species boundaries. Comparisons between data from the fine-scale transect and data (for the same set of markers) from sampling a much larger area in a different region of the cricket hybrid zone reveal consistent patterns of introgression for individual loci. The consistency in patterns of introgression between these two distant and distinct regions of the hybrid zone suggests that strong selection is acting to maintain abrupt discontinuities within the hybrid zone and that genomic regions with restricted introgression likely include genes that contribute to nonecological prezygotic barriers.
... Here, we use estimates of differential introgression for a large number of single nucleotide polymorphisms (SNPs) to identify genes that remain differentiated across a mosaic hybrid zone between the field crickets, Gryllus pennsylvanicus and Gryllus firmus. The field crickets diverged approximately 200,000 years ago (Willett et al. 1997;Maroja et al. 2009a) and hybridize in a zone composed of interspersed parental and mixed populations distributed along the eastern edge of the Appalachian mountains (Harrison and Arnold 1982). Multiple prezygotic barriers limit gene exchange between species, including habitat isolation (Harrison 1986;Rand and Harrison 1989;Harrison and Bogdanowicz 1997;Ross and Harrison 2002;Larson et al. 2013), positive assortative mating (Maroja et al. 2009b), and asymmetrical postmating prezygotic barriers (Harrison 1983). ...
... data). Within the hybrid zone F1 hybrids are rare, but multigeneration backcrosses are common, indicating that there is on-going gene flow despite prezygotic barriers (Harrison 1986;Harrison and Bogdanowicz 1997;Maroja et al. 2009a;Larson et al. 2013). ...
... Previous attempts to identify divergent genes between the two cricket species have met with little success (e.g., Harrison and Bogdanowicz 1997;Broughton and Harrison 2003). However, analysis of genes encoding seminal fluid proteins (SFPs) has not only shown such genes to be rapidly evolving, but several SFP loci show major allele frequency differences between the species (Andrés et al. 2006(Andrés et al. , 2008Maroja et al. 2009a). Seminal fluid proteins are synthesized in the male accessory gland and transferred to females as part of the ejaculate. ...
Article
Hybrid zones act as genomic sieves. Although globally advantageous alleles will spread throughout the zone and neutral alleles can be freely exchanged between species, introgression will be restricted for genes that contribute to reproductive barriers or local adaptation. Seminal fluid proteins (SFPs) are known to contribute to reproductive barriers in insects and have been proposed as candidate barrier genes in the hybridizing field crickets Gryllus pennsylvanicus and Gryllus firmus. Here, we have used 125 single nucleotide polymorphisms to characterize patterns of differential introgression and to identify genes that may contribute to prezygotic barriers between these species. Using a transcriptome scan of the male cricket accessory gland (the site of SFP synthesis), we identified genes with major allele frequency differences between the species. We then compared patterns of introgression for genes encoding SFPs with patterns for genes expressed in the same tissue that do not encode SFPs. We find no evidence that SFPs have reduced gene exchange across the cricket hybrid zone. However, a number of genes exhibit dramatically reduced introgression, and many of these genes encode proteins with functional roles consistent with known barriers.
... The known hybrid zone between G. pennsylvanicus and G. firmus stretches from southern Connecticut to Virginia along the eastern slopes of the Appalachian, Blue Ridge, and Northern Highland Mountains (Harrison and Arnold 1982) (Fig. 1). The glacial history of the northeastern United States and the distribution of Gryllus mitochondrial DNA (mtDNA) haplotypes provide strong evidence that the hybrid zone formed as a result of secondary contact between lineages that diverged in allopatry (Harrison et al. 1987; Willett et al. 1997; Maroja et al. 2009a ). Gryllus pennsylvanicus extends west from the Appalachian and Blue Ridge Mountains and through the mountains to the south. ...
... In the south, G. firmus is multivoltine and females lay both diapause and non-diapause eggs (Fulton 1952; Alexander 1968; Walker 1980). The two cricket species diverged about 200,000 ya (Willett et al. 1997; Maroja et al. 2009a). They are very similar morphologically and were considered part of a single variable species until the 1950s (Fulton 1952; Alexander 1957 ). ...
... In the fall of 2010, we collected 104 crickets from nine localities in the northeastern range of G. firmus and G. pennsylvanicus. To these, we added 26 crickets from four localities collected by Maroja et al. (2009a). We also used mitochondrial DNA (mtDNA) sequence data for 98 crickets from 28 localities described in Willett et al. (1997) and Maroja et al. (2009a) (Table S1 ). ...
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Article
Hybrid zones provide insight into the nature of species boundaries and the evolution of barriers to gene exchange. Characterizing multiple regions within hybrid zones is essential for understanding both their history and current dynamics. Here, we describe a previously uncharacterized region of a well-studied hybrid zone between two species of field crickets, Gryllus pennsylvanicus and G. firmus. We use a combination of mitochondrial DNA sequencing, morphological data, and modeling of environmental variables to identify the ecological factors structuring the hybrid zone and define patterns of hybridization and introgression. We find an association between species distribution and natural habitat; Gryllus pennsylvanicus occupies natural habitat along forest edges and natural clearings, whereas G. firmus occupies more disturbed areas in agricultural and suburban environments. Hybridization and introgression occur across patch boundaries; there is evidence of substantial admixture both in morphological characters and mtDNA, over a broad geographic area. Nonetheless, the distribution of morphological types is bimodal. Given that F1 hybrids are viable and fertile in the lab, this suggests that strong pre-zygotic barriers are operating in this portion of the hybrid zone.
... Here we combine the candidate gene and genome-scan approaches, using high-throughput sequencing to survey the male accessory gland transcriptomes of two closely related species of field crickets that interact in a well-characterized hybrid zone in North America. The two cricket species (Gryllus firmus and Gryllus pennsylvanicus) are estimated to have diverged 200,000 years ago (Broughton and Harrison 2003;Maroja et al. 2009). Attempts to identify fixed differences between the species have met with only limited success. ...
... These data suggest that much of the field cricket genome has remained undifferentiated following the origin of reproductive barriers. In contrast, recent proteomic analysis of spermatophore contents identified two SFP genes that exhibit nearly fixed differences and strong evidence that positive selection has been responsible for patterns of differentiation (Andres et al. 2008;Maroja et al. 2009). ...
... Selecting these highly divergent contigs allowed us to validate putative regions of genomic differentiation between the two crickets. In addition, we generated gene genealogies for this subset of genes and compared them with the genealogies of two highly differentiated SFP genes (AG-0005F and AG-0334P) that show almost exclusive relationships between the two species (Andrés et al. 2008;Maroja et al. 2009). ...
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Article
One of the central questions in evolutionary genetics is how much of the genome is involved in the early stages of divergence between populations, causing them to be reproductively isolated. In this paper we investigate genomic differentiation in a pair of closely related field crickets (Gryllus firmus and G. pennsylvanicus). These two species are the result of allopatric divergence and now interact along an extensive hybrid zone in eastern North America. Genes encoding seminal fluid proteins (SFPs) are often divergent between species and it has been hypothesized that these proteins may play a key role in the origin and maintenance of reproductive isolation between diverging lineages. Hence, we chose to scan the accessory gland transcriptome to enable direct comparisons of differentiation for genes known to encode SFPs with differentiation at a much larger set of genes expressed in the same tissue. We have characterized differences in allele frequency between two populations for >6,000 SNPs and >26,000 contigs. About 10% of all SNPs showed nearly fixed differences between the two species. Genes encoding SFPs did not have significantly elevated numbers of fixed SNPs per contig, nor do they seem to show larger differences than expected in their average allele frequencies. The distribution of allele frequency differences across the transcriptome is distinctly bimodal, but the relatively high proportion of fixed SNPs does not necessarily imply "ancient" divergence between these two lineages. Further studies of linkage disequilibrium and introgression across the hybrid zone are needed to direct our attention to those genome regions that are important for reproductive isolation.
... The field crickets G. firmus and G. pennsylvanicus interact in a well-characterized hybrid zone stretching from Connecticut to North Carolina, along the eastern edge of the Appalachian Mountains (Harrison & Arnold, 1982). Where the two species co-occur, F1 hybrids are rare, but individuals of mixed ancestry are common (Harrison & Bogdanowicz, 1997;Maroja et al., 2009b). Because female field crickets are promiscuous, and mate with many different males (Solymar & Cade, 1990;Bretman & Tregenza, 2005), there is the potential for post-copulatory sexual selection. ...
... During copulation, males transfer to the female a single spermatophore containing sperm and seminal fluid, which the female stores in an elastic spermatheca that expands to hold the ejaculates from multiple males (reviewed in Zuk & Simmons, 1997). Seminal fluid proteins contained within the spermatophore have been identified, and some of the genes that encode these proteins are evolving rapidly under positive selection and are strikingly divergent between the two species (André s et al., , 2008Braswell et al., 2006;Maroja et al., 2009b). ...
... The failure of G. pennsylvanicus sperm to successfully fertilize G. firmus females could be the result of divergence in male reproductive proteins that mediate these steps or in the interaction of these proteins with the female reproductive tract. Comparisons between G. pennsylvanicus and G. firmus provide evidence that cricket reproductive proteins diverge rapidly under positive selection (André s et al., , 2008Braswell et al., 2006;Maroja et al., 2009b). ...
Article
Studies of sexual selection in speciation have traditionally focused on mate preference, with less attention given to traits that act between copulation and fertilization. However, recent work suggests that post-mating prezygotic barriers may play an important role in speciation. Here, we evaluate the role of such barriers in the field crickets, Gryllus firmus and Gryllus pennsylvanicus. Gryllus pennsylvanicus females mated with G. firmus males produce viable, fertile offspring, but when housed with both species produce offspring sired primarily by conspecifics. We evaluate patterns of sperm utilization in doubly mated G. pennsylvanicus females and find no evidence for conspecific sperm precedence. The reciprocal cross (G. firmus female × G. pennsylvanicus male) produces no progeny. Absence of progeny reflects a barrier to fertilization rather than reduced sperm transfer, storage or motility. We propose a classification scheme for mechanisms underlying post-mating prezygotic barriers similar to that used for premating barriers.
... This is especially critical in the case of introgression. If introgression is heterogeneous in a predictable way across the genome (e.g., Harrison 1990;Rieseberg et al. 1999;Wu 2001), we may be able to select classes of markers and compare patterns of variation among them that allow us to illuminate various aspects of the biology of diversification, including phylogenetic history and reticulate evolution (e.g., Carling and Brumfield 2009;Maroja et al. 2009;Petit and Excoffier 2009). Here we take this approach to phylogeny estimation in a well-studied group of rodents, the diverse chipmunks of western North America (Tamias), comparing patterns at three reproductive protein genes, one anonymous locus, and one mitochondrial gene. ...
... Here we explore the use of reproductive-protein genes, which are expected to be both resistant to introgression (e.g., Rieseberg et al. 1999;Maroja et al. 2009), and to evolve rapidly (e.g., Swanson et al. 2003), to estimate the phylogeny of a rapid mammalian radiation and test hypotheses about introgressive hybridization among its species. We examine patterns of variation at multiple nuclear loci using coalescent-based speciestree estimation methods and concatenation to estimate a species tree, use parametric bootstraps to assess the effects of mutational variance and coalescent simulations to differentiate between coalescent stochasticity and introgressive hybridization. ...
... Zp2 has previously been used in a phylogenetic context in rodents (Turner and Hoekstra 2006). We focused on these nuclear regions because three of them are found in reproductive-protein genes, which may be resistant to introgression (e.g., Rieseberg et al. 1999;Maroja et al. 2009) and are expected to be rapidly evolving (e.g., Swanson et al. 2003). ACR is a protease in the sperm acrosome that lyses the zonapellucida and facilitates the penetration of the sperm by the egg; ZAN is a transmembrane sperm protein that functions in the binding of sperm the zonapellucida; Zp2 is an egg protein in the zona pellucida that participates in sperm binding (Wasserman et al. 2001). ...
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Article
The causes and consequences of rapid radiations are major unresolved issues in evolutionary biology. This is in part because phylogeny estimation is confounded by processes such as stochastic lineage sorting and hybridization. Because these processes are expected to be heterogeneous across the genome, comparison among marker classes may provide a means of disentangling these elements. Here we use introns from nuclear-encoded reproductive protein genes expected to be resistant to introgression to estimate the phylogeny of the western chipmunks (Tamias: subgenus: Neotamias), a rapid radiation that has experienced introgressive hybridization of mitochondrial DNA (mtDNA). We analyze the nuclear loci using coalescent-based species-tree estimation methods and concatenation to estimate a species tree and we use parametric bootstraps and coalescent simulations to differentiate between phylogenetic error, coalescent stochasticity and introgressive hybridization. Results indicate that the mtDNA gene tree reflects several introgression events that have occurred between taxa of varying levels of divergence and at different time points in the tree. T. panamintinus and T. speciosus appear to be fixed for ancient mitochondrial introgressions from T. minimus. A southern Rocky Mountains clade appears well sorted (i.e., species are largely monophyletic) at multiple nuclear loci, while five of six taxa are nonmonophyletic based on cytochrome b. Our simulations reject phylogenetic error and coalescent stochasticity as causes. The results represent an advance in our understanding of the processes at work during the radiation of Tamias and suggest that sampling reproductive-protein genes may be a viable strategy for phylogeny estimation of rapid radiations in which reproductive isolation is incomplete. However, a genome-scale survey that can statistically compare heterogeneity of genealogical process at many more loci will be necessary to test this conclusion.
... Four priors calibrated the analysis to geologic time. Two normally distributed priors were based upon molecular divergence time estimates: the divergence of Florida G. firmus from G. pennsylvanicus had a prior of 1.25 ± 0.25 MYA, based on a estimate of 0.2 MYA from mtDNA (Maroja et al. 2009) but potentially up to 2 MYA based on ~100 loci nDNA (L. Maroja, pers. ...
... The eastern G. firmus-G. pennsylvanicus species pair have been the subject of extensive evolutionary genetic analyses (Larson et al. 2013(Larson et al. , 2014Maroja et al. 2009Maroja et al. , 2015; clearly the situation described here calls for future work along the boundary between G. pennsylvanicus and what is currently called G. firmus in Texas (see Weissman & Gray 2019 p. 61 for further discussion). ...
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Article
We present the first comprehensive molecular phylogeny of Gryllus field cricket species found in the United States and Canada, select additional named Gryllus species found in Mexico and the Bahamas, plus the European field cricket G. campestris Linnaeus and the Afro-Eurasian cricket G. bimaculatus De Geer. Acheta, Teleogryllus, and Nigrogryllus were used as outgroups. Anchored hybrid enrichment was used to generate 492,531 base pairs of DNA sequence from 563 loci. RAxML analysis of concatenated sequence data and Astral analysis of gene trees gave broadly congruent results, especially for older branches and overall tree structure. The North American Gryllus are monophyletic with respect to the two Old World taxa; certain sub-groups show rapid recent divergence. This is the first Anchored Hybrid Enrichment study of an insect group done for closely related species within a single genus, and the results illustrate the challenges of reconstructing the evolutionary history of young rapidly diverged taxa when both incomplete lineage sorting and probable hybridization are at play. Because Gryllus field crickets have been used extensively as a model system in evolutionary ecology, behavior, neuro-physiology, speciation, and life-history and life-cycle evolution, these results will help inform, interpret, and guide future research in these areas.
... Since mtDNA does not recombine it behaves as a single locus, therefore studies relying solely on this marker will provide only one gene tree among all other possibilities in the evolutionary process. The mitochondrial gene tree may differ from the species tree not only due to deep coalescence, but also because of hybridization and introgression events ; see examples in and Maroja et al., 2009;and Shaw, 2002). The disadvantages of analysing one gene are valid not only for studies focused on several mtDNA genes, but also when one uses a single nuclear marker. ...
... We recovered a well-supported mtDNA phylogenetic tree for North African Tarentola (Fig. IV.1), adding considerable information to what was initially estimated in Article I and to the general knowledge about this genus . However, the mitochondrial gene tree can differ from the species tree not only because of deep coalescence, but also because of hybridization and introgression events ; see examples in and Maroja et al., 2009;and Shaw, 2002). ...
... Selection on genes that underlie mating specificity and mate recognition may play an important role in the evolution of nongeographic barriers to gene flow between populations diverging in key phenotypic or life history traits that involve interactions between individuals, such as mating behavior (Martin and Hosken 2004), host choice (Hawthorne and Via 2001;Messina and Jones 2011), and mate signaling (color and vision, Kronforst et al. 2006;biochemical, Smadja and Butlin 2008), or interactions between gametes such as cognate proteins involved in fertilization specificity (Clark et al. 2006;Vacquier and Swanson 2011;Sunday and Hart 2013). Genes encoding compatibility proteins have been shown to evolve rapidly in diverse groups of animals and plants Clark et al. 2006;Turner and Hoekstra 2008), and the rapid divergence of interacting proteins involved in reproduction has also been implicated in the maintenance of species boundaries during hybridization in mammals (Paysuer and Nachman 2005) and insects (Maroja et al. 2009), and in reproductive incompatibilities between closely related species of marine invertebrates (e.g., Vacquier 1998;Hellberg and Vacquier 1999;Zigler et al. 2005;Clark et al. 2009). ...
... Genes encoding reproductive compatibility proteins have been shown to evolve rapidly under positive selection and have been implicated in the primary divergence among conspecific populations (e.g., Sunday and Hart 2013;Hart et al. 2014) and in the maintenance of reproductive boundaries between already diverged, hybridizing species in sympatry (e.g., Maroja et al. 2009). We describe the gene coding for bindin for all three sea star species in the genus Pisaster and analyze its molecular evolution within and between species. ...
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Article
Reproductive compatibility proteins have been shown to evolve rapidly under positive selection leading to reproductive isolation, despite the potential homogenizing effects of gene flow. This process has been implicated in both primary divergence among conspecific populations and reinforcement during secondary contact; however, these two selective regimes can be difficult to discriminate from each other. Here, we describe the gene that encodes the gamete compatibility protein bindin for three sea star species in the genus Pisaster. First, we compare the full-length bindin-coding sequence among all three species and analyze the evolutionary relationships between the repetitive domains of the variable second bindin exon. The comparison suggests that concerted evolution of repetitive domains has an effect on bindin divergence among species and bindin variation within species. Second, we characterize population variation in the second bindin exon of two species: We show that positive selection acts on bindin variation in Pisaster ochraceus but not in Pisaster brevispinus, which is consistent with higher polyspermy risk in P. ochraceus. Third, we show that there is no significant genetic differentiation among populations and no apparent effect of sympatry with congeners that would suggest selection based on reinforcement. Fourth, we combine bindin and cytochrome c oxidase 1 data in isolation-with-migration models to estimate gene flow parameter values and explore the historical demographic context of our positive selection results. Our findings suggest that positive selection on bindin divergence among P. ochraceus alleles can be accounted for in part by relatively recent northward population expansions that may be coupled with the potential homogenizing effects of concerted evolution.
... Patterns of differential introgression have frequently been documented for hybrid zones (e.g., Harrison 1990;Rieseberg et al. 1999;Payseur et al. 2004;Payseur and Nachman 2005;Teeter et al. 2008Teeter et al. , 2010Maroja et al. 2009;Macholan et al. 2011), and these patterns provide direct evidence that gene exchange cannot be viewed as a property of the genome as a whole. The early literature relied on morphological, allozyme, and organelle DNA data; multilocus DNA sequence data were not yet available. ...
... Multilocus sequence data have provided repeated examples of discordance among gene genealogies of closely related species or subspecies (e.g., Ting et al. 2000, Beltrán et al. 2002Machado and Hey 2003;Dopman et al. 2005;Putnam et al. 2007;Andres et al 2008;Maroja et al. 2009;White et al. 2009;Lassance et al. 2011). Genealogical discordance often appears to be the result of ancestral polymorphism and lineage sorting, but in other cases it would seem to be a consequence of recent hybridization and differential introgression (Shaw 2002;Ohshima and Yoshikawa 2010). ...
Article
The literature on speciation has expanded dramatically in recent years, catalyzed by the emergence of new conceptual frameworks, new theoretical approaches, and new methods for characterizing pattern and inferring process. As a consequence, the language used to describe the speciation process has become more complex. Increasing complexity may be an accurate reflection of current thinking with respect to how phenotypic differences limit gene flow, how selection results in the evolution of reproductive isolation, and genetic changes that contribute to speciation. However, increased language complexity has come at a cost; old definitions have been reconfigured and new terms have been introduced. In some instances, the introduction of new terminology has failed to recognize historical usage, leading to unnecessary ambiguity and redundancy. Although the writings of Mayr and Dobzhansky remain a reference point in the language of speciation, the last decades of the 20th century saw substantial changes in our thinking about the speciation process. During that period, the language of speciation remained relatively stable. In contrast, the first decade of the 21st century has witnessed a remarkable expansion of the language of speciation. Here, the origin and evolution of ideas about speciation are viewed through the lens of changing language use.
... Like this, other studies have utilized the field crickets G. firmus and G. pennsylvanicus, which interact and form a hybrid zone in the Eastern USA. They diverged more recently, 200,000 years ago, and there is an ongoing gene flow despite prezygotic barriers (Maroja et al. 2009;Larson et al. 2013). Transcriptomic scan from individuals in a hybrid zone reveals candidate prezygotic barrier genes with remarkably reduced introgression including ones encoding cytoskeletal proteins, which are involved in critical steps in fertilization Larson et al. 2013). ...
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Article
Significant advances in biophysical methods such as next-generation sequencing technologies have now opened the way to conduct evolutionary and applied research based on the genomic information of greatly diverse insects. Crickets belonging to Orthoptera (Insecta: Polyneoptera), one of the most flourishing groups of insects, have contributed to the development of multiple scientific fields including developmental biology and neuroscience and have been attractive targets in evolutionary ecology for their diverse ecological niches. In addition, crickets have recently gained recognition as food and feed. However, the genomic information underlying their biological basis and application research toward breeding is currently underrepresented. In this review, we summarize the progress of genomics of crickets. First, we outline the phylogenetic position of crickets in insects and then introduce recent studies on cricket genomics and transcriptomics in a variety of fields. Furthermore, we present findings from our analysis of polyneopteran genomes, with a particular focus on their large genome sizes, chromosome number, and repetitive sequences. Finally, how the cricket genome can be beneficial to the food industry is discussed. This review is expected to enhance greater recognition of how important the cricket genomes are to the multiple biological fields and how basic research based on cricket genome information can contribute to tackling global food security. Supplementary information: The online version contains supplementary material available at 10.1007/s12551-021-00924-4.
... The field crickets Gryllus firmus and Gryllus pennsylvanicus are an excellent system in which to study the genetic architecture of introgressing and non-introgressing loci. These crickets form an extensive, well-characterized hybrid zone with multiple barriers to gene exchange including many prezygotic barriers and a one-way reproductive incompatibility, likely a post-mating, prezygotic barrier [1,2,3,4,5]. The pair of species diverged recently (~200,000 years) and 110 loci have been characterized in two locations in the hybrid zone [5,6]. ...
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Article
The genomic architecture of barriers to gene exchange during the speciation process is poorly understood. The genomic islands model suggests that loci associated with barriers to gene exchange prevent introgression of nearby genomic regions via linkage disequilibrium. But few analyses of the actual genomic location of non-introgressing loci in closely related species exist. In a previous study Maroja et al. showed that in the hybridizing field crickets, Gryllus firmus and G. pennsylvanicus, 50 non-introgressing loci are localized on two autosomal regions and the X chromosome, but they were not able to map the loci along the X chromosome because they used a male informative cross. Here, we localize the introgressing and non-introgressing loci on the X chromosome, and reveal that all X-linked non-introgressing loci are restricted to a 50-cM region with 10 of these loci mapped to a single location. We discuss the implications of this finding to speciation.
... There is considerable evidence to support this suggestion. For example, studies in hybrid zones have commonly found variation in the degree to which different loci introgress (Larson, White, Ross, & Harrison, 2014;Maroja, Andrés, Harrison, 2009;Payseur, Krenz, & Nachman, 2004;Teeter et al., 2008), a pattern which has been interpreted as due to variation in the strength of divergent selection opposing gene flow. Many studies have also used genome scans to document the spatial pattern of variation in divergence and have found genomic regions that show substantial divergence compared to the remainder of the genome (Carneiro et al., 2014;Ellegren et al., 2012;Gagnaire, Normandeay, Pavey, & Bernatchez, 2013;Harr, 2006;Hohenlohe, Bassham, Currey, & Cresko, 2012;Hohenlohe et al., 2010;Nadeau et al., 2012;White, Cheng, Simard, Costantini, & Besansky, 2010). ...
Article
Gene flow is thought to impede genetic divergence and speciation by homogenizing genomes. Recent theory and research suggest that sufficiently strong divergent selection can overpower gene flow, leading to loci that are highly differentiated compared to others. However, there are also alternative explanations for this pattern. Independent evidence that loci in highly differentiated regions are under divergent selection would allow these explanations to be distinguished, but such evidence is scarce. Here we present multiple lines of evidence that many of the highly divergent SNPs in a pair of sister morning glory species, Ipomoea cordatotriloba and I. lacunosa, are the result of divergent selection in the face of gene flow. We analyzed a SNP dataset across the genome to assess the amount of gene flow, resistance to introgression, and patterns of selection on loci resistant to introgression. We show that differentiation between the two species is much lower in sympatry than in allopatry, consistent with interspecific gene flow in sympatry. Gene flow appears to be substantially greater from I. lacunosa to I. cordatotriloba than in the reverse direction, resulting in sympatric and allopatric I. cordatotriloba being substantially more different than sympatric and allopatric I. lacunosa. Many SNPs highly differentiated in allopatry have experienced divergent selection, and despite gene flow in sympatry, resist homogenization in sympatry. Finally, five out of eight floral and inflorescence characteristics measured exhibit asymmetric convergence in sympatry. Consistent with the pattern of gene flow, I. cordatotriloba traits become much more like those of I. lacunosa than the reverse. Our investigation reveals the complex interplay between selection and gene flow that can occur during the early stages of speciation. This article is protected by copyright. All rights reserved.
... The unique role of speciation genes in establishing species boundaries has also led to arguments asserting that these genes should be especially informative about species relationships (Ting et al. 2000;Rosenberg 2003;Maroja et al. 2009;Zachos 2009;Nosil and Schluter 2011;Cutter 2013). Such a property becomes useful when multiple species are separated by very short times between successive speciation events. ...
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Article
Speciation genes are responsible for reproductive isolation between species. By directly participating in the process of speciation, the genealogies of isolating loci have been thought to more faithfully represent species trees. The unique properties of speciation genes may provide valuable evolutionary insights and help determine the true history of species divergence. Here, we formally analyze whether genealogies from loci participating in Dobzhansky–Muller (DM) incompatibilities are more likely to be concordant with the species tree under incomplete lineage sorting (ILS). Individual loci differ stochastically from the true history of divergence with a predictable frequency due to ILS, and these expectations—combined with the DM model of intrinsic reproductive isolation from epistatic interactions—can be used to examine the probability of concordance at isolating loci. Contrary to existing verbal models, we find that reproductively isolating loci that follow the DM model are often more likely to have discordant gene trees. These results are dependent on the pattern of isolation observed between three species, the time between speciation events, and the time since the last speciation event. Results supporting a higher probability of discordance are found for both derived–derived and derived–ancestral DM pairs, and regardless of whether incompatibilities are allowed or prohibited from segregating in the same population. Our overall results suggest that DM loci are unlikely to be especially useful for reconstructing species relationships, even in the presence of gene flow between incipient species, and may in fact be positively misleading.
... In field crickets, closely related species often occur sympatrically and are morphologically and ecologically cryptic, but show strong differentiation in the male acoustic mating signals and corresponding female preferences . This makes them ideal subjects for the study of speciation with historic and/or secondary gene flow (Maroja et al. 2009. Genomic resources for crickets are still scarce (Danley et al. 2007) but rapidly expanding through de novo transcriptome assembly (Zeng et al. 2013. ...
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Die vorliegende Dissertation verbindet Ergebnisse aus neuroethologischen, verhaltensbiologischen, quantitativ genetischen und genomischen Ansätzen bei Feldgrillen (Gryllus), um neue Erkenntnisse über die Rolle von sexueller Selektion bei Artbildung zu erlangen. Es wird gezeigt dass multivariate Gesangspräferenzen von Grillenweibchen von wenigen Merkmalen abhängen und zwischen Arten ähnlich sind, während sich Männchengesänge in allen Merkmalen unterschieden. Verschiedene Ebenen der Gesangserkennung sind durch unterschiedliche Präferenzfunktionen charakterisiert. Multivariate Präferenzen können also gleichzeitig verschiedene Indikatoren für Paarungspartnerqualität aus den Gesangsmerkmalen erkennen. Eine polygene genetische Architektur der Gesangsmerkmale und der Präferenz wurde beobachtet und weist auf eine eher langsamere Divergenz hin, obwohl gonosomale Vererbung mehrerer Gesangsmerkmale höhere Evolutionsraten zulässt. Starke Kovarianz zwischen den Merkmalen die direkt sexueller Selektion unterliegen und Merkmale, die nicht direkt von Weibchen gewählt werden, zeigen, dass indirekte Selektion teilweise für die markante Divergenz der Gesänge verantwortlich sein könnte, trotz begrenzter Divergenz der Präferenzen. Ferner zeigte ein Artvergleich der multivariaten Gesangsmerkmale, dass die Form der Präferenzfunktion die Ausrichtung der Kovarianzen und damit die erwartete Selektionsantwort der männlichen Gesänge beeinflussen kann. Simulationen ergaben starke Hinweise auf Genfluss zwischen zwei nahverwandten Arten über einen langen Zeitraum . Nur wenige Contigs zeigten hohe genetische Divergenz und hohe Raten nicht-synonymer Polymorphismen. Diese stimmten aber mit Genen überein, die experimentell nachgewiesene Funktionen in neuromuskulärer Entwicklung und im Paarungsverhalten haben. Zusammen zeigen die Ergebnisse das Potential von sexueller Selektion bei der Entstehung und Aufrechterhaltung von reproduktiver Isolation zwischen Arten.
... Traits under different selection regimes are expected to introgress across species boundaries at different rates (Harrison 1990;Mallet 2005;Yuri et al. 2009). For example, attributes under neutral or positive selection are expected to introgress more so than traits under divergent selection (Gay et al. 2009;Maroja et al. 2009;). ...
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Unstable hybrid swarms that arise following the introduction of non-native species can overwhelm native congeners, yet the stability of invasive hybrid swarms has not been well documented over time. Here, we examine genetic variation and clinal stability across a recently formed hybrid swarm involving native blacktail shiner (Cyprinella venusta) and non-native red shiner (C. lutrensis) in the Upper Coosa River basin, which is widely considered to be a global hot spot of aquatic biodiversity. Examination of phenotypic, multilocus genotypic, and mitochondrial haplotype variability between 2005 and 2011 revealed that the proportion of hybrids has increased over time, with more than a third of all sampled individuals exhibiting admixture in the final year of sampling. Comparisons of clines over time indicated that the hybrid swarm has been rapidly progressing upstream, but at a declining and slower pace than rates estimated from historical collection records. Clinal comparisons also showed that the hybrid swarm has been expanding and contracting over time. Additionally, we documented the presence of red shiner and hybrids farther downstream than prior studies have detected, which suggests that congeners in the Coosa River basin, including all remaining populations of the threatened blue shiner (Cyprinella caerulea), are at greater risk than previously thought.
... Speciation genes are more likely to become fixed for species-specific alleles early in the process of speciation, and therefore are expected to be relatively exempt from incomplete sorting and subject to reduced introgression (Wu, 2001; Feder, Egan & Nosil, 2012). Similar patterns have been observed in Drosophila, field crickets, and moths (Ting, Tsaur & Wu, 2000; Dopman et al., 2005; Maroja, Andrés & Harrison, 2009; Andrés et al., 2013; Larson et al., 2013). It is possible that these genes are not the direct targets but rather linked to targets of divergent selection as the interaction between linkage and selection makes it challenging to distinguish between recurrent positive selection, background selection, and Hill–Robertson effects (Hill & Robertson, 1966; Charlesworth, 1994; Andolfatto, 2007; Charlesworth et al., 2009). ...
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In the Allonemobius socius complex of crickets, reproductive isolation is primarily accomplished via postmating prezygotic barriers. We tested seven protein-coding genes expressed in the male ejaculate for patterns of evolution consistent with a putative role as postmating prezygotic isolation genes.Our recently diverged species generally lacked sequence variation. As a result, ω -based tests were only mildly successful. Some of our genes showed evidence of elevated ω values on the internal branches of gene trees. In a couple genes these internal branches coincided with both species branching events of the species tree, between A. fasciatus and the other two species, and between A. socius and A. sp. nov. Tex. In comparison, more successful approaches were those that took advantage of the varying degrees of lineage sorting and allele sharing among our young species. These approaches were particularly powerful within the contact zone. Among the genes we tested we found genes with genealogies that indicated relatively advanced degrees of lineage sorting across both allopatric and contact zone alleles. Within a contact zone between two members of the species complex, only a subset of genes maintained allelic segregation despite evidence of ongoing gene flow in other genes. The overlap in these analyses was arginine kinase (AK) and apolipoprotein A-1 binding protein (APBP). These genes represent two of the first examples of sperm maturation, capacitation, and motility proteins with fixed non-synonymous substitutions between species-specific alleles that may lead to postmating prezygotic isolation. Both genes express ejaculate proteins transferred to females during copulation and were previously identified through comparative proteomics. We discuss the potential function of these genes in the context of the specific postmating prezygotic isolation phenotype among our species, namely conspecific sperm precedence and the superior ability of conspecific males to induce oviposition in females.
... Using comparison of transcriptomes from male accessory glands of the two cricket species, we identified 9731 SNPs, most of which showed little differentiation between species (Andr es et al. 2013), consistent with previous studies in which divergence time estimates of about 200 000 years were obtained from analysis of differentiation for mtDNA and a small number of nuclear genes (e.g. Maroja et al. 2009). A subset of the highly differentiated SNPs (D > 0.8, where D is the allele frequency difference between allopatric populations of the two species) were used in geographic and genomic cline analyses for two transects/regions of the hybrid zone (Larson et al. 2013a(Larson et al. ,b, 2014. ...
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Hybrid zones have been promoted as windows on the evolutionary process and as laboratories for studying divergence and speciation. Patterns of divergence between hybridizing species can now be characterized on a genome-wide scale, and recent genome scans have focused on the presence of "islands" of divergence. Patterns of heterogeneous genomic divergence may reflect differential introgression following secondary contact and provide insights into which genome regions contribute to local adaptation, hybrid unfitness, and positive assortative mating. However, heterogeneous genome divergence can also arise in the absence of any gene flow, as a result of variation in selection and recombination across the genome. We suggest that to understand hybrid zone origins and dynamics, it is essential to distinguish between genome regions that are divergent between pure parental populations and regions that show restricted introgression where these populations interact in hybrid zones. The latter, more so than the former, reveal the likely genetic architecture of reproductive isolation. Mosaic hybrid zones, because of their complex structure and multiple contacts, are particularly good subjects for distinguishing primary intergradation from secondary contact. Comparisons among independent hybrid zones or transects that involve the "same" species pair can also help to distinguish between divergence with gene flow and secondary contact. However, data from replicate hybrid zones or replicate transects do not reveal consistent patterns; in a few cases, patterns of introgression are similar across independent transects, but for many taxa, there is distinct lack of concordance, presumably due to variation in environmental context and/or variation in the genetics of the interacting populations. This article is protected by copyright. All rights reserved.
... loci (Dopman et al., 2005;Kronforst et al., 2006;Maroja et al., 2009;Ohshima and Yoshizawa, 2010;Baldassarre et al., 2014;Taylor et al., 2014). Such differential introgression has commonly been attributed to the effects of natural selection or genetic drift, but may also reflect variable recombination rates due to structural features such as chromosome inversions (reviewed inNachman and Payseur, 2012) , or differences in the extent of linkage between genetic markers and genes under divergent selection (Payseur et al., 2004). ...
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Observations that rates of introgression between taxa can vary across loci are increasingly common. Here we test for differential locus-wise introgression in two parapatric subspecies of Pearson′s horseshoe bat (Rhinolophus pearsoni chinensis and R. p. pearsoni). To efficiently identify putative speciation genes and/or beneficial genes in our current system, we used a candidate gene approach by including loci from X chromosome that are suggested to be more likely involved in reproductive isolation in other organisms and loci underlying hearing that have been suggested to spread across the hybrid zone in another congeneric species. Phylogenetic and coalescent analyses were performed at two X-linked, four hearing genes, as well as two other autosomal loci individually. Likelihood ratio tests could not reject the model of zero gene flow at two X-linked and two autosomal genes. In contrast, gene flow was supported at three of four hearing genes. While this introgression could be adaptive, we cannot rule out stochastic processes. Our results highlight the utility of the candidate gene approach in searching for speciation genes and/or beneficial genes across the species boundary in natural populations.
... Introgressive hybridization is a common phenomenon in the Anopheline species (Davidson 1964, White 1971, Temu et al. 1997, Slotman et al. 2005, and recent studies have reported the presence of natural hybrids of An. sinensis s.s. and the sister species An. kleini in the ROK (Joshi et al. 2009a). The reason that mtDNA could not indicate this genetic introgression may be owing to asymmetric introgression, which has been documented in a variety of insects, such as the Anopheles gambiae complex (Besansky et al. 2003), Heliconius butterflies (Kronforst et al. 2006), and Gryllus crickets (Maroja et al. 2009). The previous hybridization experiments showed asymmetric introgression even in the An. ...
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Anopheles sinensis Wiedemann sensu stricto (s.s.) is a dominant mosquito and considered a secondary malaria vector in the Republic of Korea (ROK). Despite the potential significance for malaria control, population genetics studies have been conducted using only mitochondrial DNA (mtDNA), and studies of the genetics of hybridization have never been attempted. In this study, 346 specimens from 23 localities were subject to experiments. Among them, 305 An. sinensis s.s. specimens from 20 localities were used for mtDNA analysis, and 346 specimens comprising 341 An. sinensis s.s. from 22 localities and five Anopheles kleini Rueda from one locality were examined in the microsatellite study. Neighbor-joining analysis of pairwise FST and RST based on microsatellite results showed that the populations are divided into two groups, as did the mtDNA results. However, the Bayesian analysis and factorial correspondence analysis plots showed three distinct clusters. Among the mtDNA and microsatellite results, only microsatellites represented small but positive and significant isolation-by-distance patterns. Both molecular markers show the Taebaek and Sobaek Mountain ranges as barriers between the northern and southern parts of the ROK. The newly recognized third group suggests possible introgressive hybridization of An. sinensis s.s. with closely related species. The slightly different composition of populations in each group based on different markers is probably because of different population dynamics in each group. These results imply that there is restricted gene flow of epidemiologically important malaria-related genes between the northern and southern parts of the ROK. © The Authors 2015. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For Permissions, please email: journals.permissions@oup.com.
... Here we construct a genetic linkage map to provide the framework for evaluating patterns of differential introgression across the hybrid zone between the field crickets Gryllus firmus and Gryllus pennsylvanicus. This species pair is recently diverged (200,000 years) (Broughton and Harrison 2003;Maroja et al. 2009a), and multiple barriers to gene exchange have been well characterized. These barriers include: (1) habitat isolation (G. ...
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Characterizing the extent of genomic differentiation between recently diverged lineages provides an important context for understanding the early stages of speciation. When such lineages form discrete hybrid zones, patterns of differential introgression allow direct estimates of which genome regions are likely involved in speciation and local adaptation. Here we use a backcross experimental design to construct a genetic linkage map for the field crickets Gryllus firmus and Gryllus pennsylvanicus, which interact in a well-characterized hybrid zone in eastern North America. We demonstrate that loci with major allele frequency differences between allopatric populations are not randomly distributed across the genome. Instead most are either X-linked or map to a few small autosomal regions. Furthermore, the subset of those highly differentiated markers which exhibit restricted introgression across the cricket hybrid zone are also concentrated on the X chromosome (39 of 50 loci) and in a single 7cM region of one autosome. Although the accumulation on the sex chromosome of genes responsible for post-zygotic barriers is a well-known phenomenon, less attention has been given to the genomic distribution of genes responsible for pre-zygotic barriers. We discuss the implications of our results for speciation, both in the context of the role of sex chromosomes and also with respect to the likely causes of heterogeneous genomic divergence. While we do not yet have direct evidence for the accumulation of ecological, behavioral, or fertilization pre-zygotic barrier genes on the X chromosome, faster X evolution could make these barriers more likely to be X-linked. Copyright © 2015 Author et al.
... Stable hybrid zones form when hybridization is restricted to a narrow zone of contact between the parental species, but the genetic integrity of both parental species remains intact [35]. Hybrid zones have been identified in the wild in a variety of taxa, and have proved extremely useful in the study of the hybridization process [42][43][44][45]. Perhaps the most significant evolutionary consequence of hybridization is the transfer of genetic material between species, which potentially facilitates the rapid creation of novel genotypes and can lead to adaptive evolution [26,33,46]. ...
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Hybridization in natural populations provides an opportunity to study the evolutionary processes that shape divergence and genetic isolation of species. The emergence of pre-mating barriers is often the precursor to complete reproductive isolation. However, in recently diverged species, pre-mating barriers may be incomplete, leading to hybridization between seemingly distinct taxa. Here we report results of a long-term study at Bird Island, South Georgia, of the extent of hybridization, mate fidelity, timing of breeding and breeding success in mixed and conspecific pairs of the sibling species, Macronectes halli (northern giant petrel) and M. giganteus (southern giant petrel). The proportion of mixed-species pairs varied annually from 0.4-2.4% (mean of 1.5%), and showed no linear trend with time. Mean laying date in mixed-species pairs tended to be later than in northern giant petrel, and always earlier than in southern giant petrel pairs, and their breeding success (15.6%) was lower than that of conspecific pairs. By comparison, mixed-species pairs at both Marion and Macquarie islands always failed before hatching. Histories of birds in mixed-species pairs at Bird Island were variable; some bred previously or subsequently with a conspecific partner, others subsequently with a different allospecific partner, and some mixed-species pairs remained together for multiple seasons. We also report the first verified back-crossing of a hybrid giant petrel with a female northern giant petrel. We discuss the potential causes and evolutionary consequences of hybridization and back-crossing in giant petrels and summarize the incidence of back-crossing in other seabird species.
... For evolutionary biologists, hybrid zones offer windows on evolutionary process [9], while they provide the divergent populations themselves with a means to interact with each other. Genes can exchange due to the semi-permeable nature of the genome [10], and this in turn can result in variation in the level of introgression of alleles among different genomic regions [11][12][13][14]. ...
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Background Hybrid zones formed by the secondary contact of divergent lineages represent natural laboratories for studying the genetic basis of speciation. Here we tested for patterns of differential introgression among three X-linked and 11 autosomal regions to identify candidate loci related to either reproductive isolation or adaptive introgression across a hybrid zone between two Chinese mainland subspecies of the intermediate horseshoe bat Rhinolophus affinis: R. a. himalayanus and R. a. macrurus. Results Our results support the previous suggestion that macrurus formed when a third subspecies (R. a. hainanus) recolonized the mainland from Hainan Island, and that himalayanus is the ancestral taxon. However, this overall evolutionary history was not reflected in all loci examined, with considerable locus-wise heterogeneity seen in gene tree topologies, levels of polymorphism, genetic differentiation and rates of introgression. Coalescent simulations suggested levels of lineage mixing seen at some nuclear loci might result from incomplete lineage sorting. Isolation with migration models supported evidence of gene flow across the hybrid zone at one intronic marker of the hearing gene Prestin. Conclusions We suggest that phylogenetic discordance with respect to the species tree seen here is likely to arise via a combination of incomplete lineage sorting and a low incidence of introgression although we cannot rule out other explanations such as selection and recombination. Two X-linked loci and one autosomal locus were identified as candidate regions related to reproductive isolation across the hybrid zone. Our work highlights the importance of including multiple genomic regions in characterizing patterns of divergence and gene flow across a hybrid zone.
... In addition, studies of hybrid zones formed after secondary contact have provided major insights into the resistance of loci to introgression across such zones (e.g. Payseur et al. 2004;Kronforst et al. 2006;Teeter et al. 2008;Maroja et al. 2009). These studies generally find a small number of differentiated loci and a large number of loci with evidence of introgression. ...
Article
The metaphor of “genomic islands of speciation” was first used to describe heterogeneous differentiation among loci between the genomes of closely related species. The biological model proposed to explain these differences was that the regions showing high levels of differentiation were resistant to gene flow between species, while the remainder of the genome was being homogenized by gene flow and consequently showed lower levels of differentiation. However, the conditions under which such differentiation can occur at multiple unlinked loci are restrictive; additionally, essentially all previous analyses have been carried out using relative measures of divergence, which can be misleading when regions with different levels of recombination are compared. Here we test the model of differential gene flow by asking whether absolute divergence is also higher in the previously identified “islands.” Using five species-pairs for which full sequence data is available, we find that absolute measures of divergence are not higher in genomic islands. Instead, in all cases examined we find reduced diversity in these regions, a consequence of which is that relative measures of divergence are abnormally high. These data therefore do not support a model of differential gene flow among loci, though islands of relative divergence may represent loci involved in local adaptation. Simulations using the program IMa2 further suggest that inferences of any gene flow may be incorrect in many comparisons. We instead present an alternative explanation for heterogeneous patterns of differentiation, one in which post-speciation selection generates patterns consistent with multiple aspects of the data.This article is protected by copyright. All rights reserved.
... It is first important to recognize that reticulate evolutionary patterns may result from a variety of different population-level processes. For example, genetic introgression may occur due to the presence of either a stable or transitory hybrid zone between populations [3][4][5]. However, another potentially widespread process leading to reticulate evolutionary patterns may be that of discrete secondary contact events between previously allopatric populations. ...
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One common form of reticulate evolution arises as a consequence of secondary contact between previously allopatric populations. Using extensive coalescent simulations, we describe the conditions for, and extent of, the introgression of genetic material into the genome of a colonizing population from an endemic population. The simulated coalescent histories are sampled from models that describe the evolution of entire chromosomes, thereby allowing the expected length of introgressed haplotypes to be estimated. The results indicate that our ability to identify reticulate evolution from genetic data is highly variable and depends critically upon the duration of the period of allopatry, the timing of the secondary contact event, as well as the sizes of the populations at the time of contact. One particularly interesting result arises when secondary contact occurs close to the time of a severe founder event, in this case, genetic introgression can be substantially more difficult to detect. However, if secondary contact occurs after such a founding event, when the range of the colonizing population increases, introgression is more readily detectable across the genome. This result may have important implications for our ability to detect introgression between ancestrally bottlenecked modern human populations and archaic hominin species, such as Neanderthals.
... The hybridizing field crickets -Gryllus firmus [11] and Gryllus pennsylvanicus [12] -form an extensive hybrid zone [13][14][15][16] and have multiple barriers to gene exchange [17][18][19][20][21] including an early acting pre-mating behavioral barrier [22]. Conspecific pairs mate faster than heterospecific pairs [22] and, although male courtship behavior has never been analyzed, the time to mate barrier has been interpreted as female choice. ...
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Pre-zygotic barriers often involve some form of sexual selection, usually interpreted as female choice, as females are typically the choosier sex. However, males typically show some mate preferences, which are increasingly reported. Here we document previously uncharacterized male courtship behavior (effort and song) and cuticular hydrocarbon (CHC) profiles in the hybridizing crickets Gryllus firmus and G. pennsylvanicus. These two species exhibit multiple barriers to gene exchange that act throughout their life history, including a behavioral barrier that results in increased time to mate in heterospecific pairs. We demonstrated that male mate choice (as courtship effort allocation) plays a more important role in the prezygotic behavioral barrier than previously recognized. In gryllids females ultimately decide whether or not to mate, yet we found males were selective by regulating courtship effort intensity toward the preferred (conspecific) females. Females were also selective by mating with more intensely courting males, which happened to be conspecifics. We report no differences in courtship song between the two species and suggest that the mechanism that allows males to act differentially towards conspecific and heterospecific females is the cuticular hydrocarbon (CHC) composition. CHC profiles differed between males and females of both species, and there were clear differences in CHC composition between female G. firmus and G. pennsylvanicus but not between the males of each species. Although many barriers to gene exchange are known in this system, the mechanism behind the mate recognition leading to reduced heterospecific mating remains unknown. The CHC profiles might be the phenotypic cue that allow males to identify conspecifics and thus to adjust their courtship intensity accordingly, leading to differential mating between species.
... If resources allow for data collection from 40 or 60 individuals, significant mapping resolution could be achieved in F 2 or F 4 hybrids (Fig. 6), although genotype-phenotype association failed to provide fine resolution in laboratory crosses of these species owing to a lack of recombination in the candidate region (Martin et al. 2012). A similar investment could also be leveraged to identify ecological and behavioural ATL in the secondary-contact hybrid zone between Gryllus pennsylvanicus and Gryllus firmus crickets that show intermediate (F ST % 0.26) levels of nuclear divergence (Broughton & Harrison 2003;Maroja et al. 2009;Andr es et al. 2013). ...
Article
Mapping adaptive trait loci (ATL) underlying ecological divergence is an essential step towards understanding the processes that generate phenotypic diversity. Technological advances have made it possible to sequence exomes in non-model systems, providing an efficient means of analyzing functional genetic variants. Divergence scans of genetic markers for outlier loci, or 'divergence mapping', have been used to map locally adapted genes, but this approach is likely to be underpowered when background divergence is elevated. Genotype-phenotype association tests in admixed populations, or 'admixture mapping', may provide a useful approach for mapping locally adapted loci when neutral divergence is high. To determine the power and limits of divergence mapping, we simulated exomes containing a single ATL across two parental populations of varying neutral divergence, estimated divergence, and quantified the power to identify the ATL. We found that divergence mapping had very high power when background FST is less than 0.2, but decreased dramatically above this level. To evaluate the utility of admixture mapping, we simulated exomes from admixed populations, then simulated phenotypes, conducted genotype-phenotype association tests, and found that even two generations of random mating after admixture could provide high mapping power in scenarios where pure divergence mapping was ineffective (FST = 0.35). Moreover, admixture mapping had high power across all levels of divergence after 20 generations since admixture. Together with high-throughput exome sequencing, admixture mapping could be used to map ATL in systems such as Heliconius butterflies or Gryllus crickets when experimental design and analytical approach are chosen accordingly. This article is protected by copyright. All rights reserved.
... Yet, although many such early studies relied on maternally-inherited mitochondrial (mt)DNA markers alone (Avise, 2000), these reflect only a limited fraction of the evolutionary history of a lineage (Avise, 1994;Zhang & Hewitt, 2003;Ballard & Whitlock, 2004) and there is now a growing trend for studies of taxonomy, phylogeography, and population genetics to sample information from both mtDNA and nuclear (nc)DNA loci (Zhang & Hewitt, 2003). An emerging outcome of multilocus studies is the frequency with which different gene genealogies differ in relation to one other, as well as with known taxonomic relationships (Maroja, Andres & Harrison, 2009;Singhal & Moritz, 2012). Several scenarios have been proposed to explain these conflicts, including incomplete lineage sorting of ancestral polymorphisms (Edwards & Beerli, 2000;Barrowclough & Zink, 2009), introgressive hybridization (Funk & Omland, 2003), genetic incompatibilities between genomes (Rand,Haney & Fry, 2004), and sex-biased dispersal (Turmelle, Kunz & Sorenson, 2011). ...
Article
Phylogenetic discordance among taxa can provide powerful insights into past episodes of introgressive hybridization as well as lineage sorting. Previously we showed that the taxonomically distinct taxon Rhinolophus sinicus septentrionalis has undergone historical introgression with its sympatric sister subspecies R. s. sinicus. To examine in more detail the extent of gene flow between these two taxa, and also between these and their sister species R. thomasi, we obtained new samples from China, Myanmar and Vietnam, and combined new and published genetic data from these, R. rouxii and R. indorouxii from India. Phylogenetic analyses revealed three separate cases of discordance: between R. s. septentrionalis and adjacent populations of R. s. sinicus, between R. s. septentrionalis and R. thomasi and between eastern populations of R. s. sinicus and a newly identified lineage. In both former cases, the mtDNA introgression appears to be asymmetric, which is likely to have resulted from mating between R. s. septentrionalis females with smaller R. s. sinicus and R. thomasi males, although we cannot rule out other scenarios completely. Further conflicts between genetic data and accepted species arrangements across the genus, with paraphyly of members of the rouxii-group, suggests a need for a thorough systematic revision of relationships within this group.
... Loci under different selection regimes are expected to introgress across species boundaries at different rates (Harrison 1990;Mallet 2005;Yuri et al. 2009), with genes under divergent selection introgressing to a lesser extent than neutral or positively selected loci Maroja et al. 2009). Consistent with this idea, we found wide clines in multilocus microsatellite admixture profiles and mtDNA haplotypes relative to the cline describing variation at phenotypic traits. ...
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The erosion of species boundaries can involve rapid evolutionary change. Consequently, many aspects of the process remain poorly understood, including the formation, expansion, and evolution of hybrid swarms. Biological invasions involving hybridization present exceptional opportunities to study the erosion of species boundaries because timelines of interactions and outcomes are frequently well known. Here, we examined clinal variation across codominant and maternally inherited genetic markers as well as phenotypic traits to characterize the expansion and evolution of a hybrid swarm between native Cyprinella venusta and invasive Cyprinella lutrensis minnows. Discordant introgression of phenotype, microsatellite multilocus genotype, and mtDNA haplotype indicates that the observable expansion of the C. venusta × C. lutrensis hybrid swarm is a false invasion front. Both parental and hybrid individuals closely resembling C. lutrensis are numerically dominant in the expansion wake, indicating that the non‐native parental phenotype may be selectively favored. These findings show that cryptic introgression can extend beyond the phenotypic boundaries of hybrid swarms and that hybrid swarms likely expand more rapidly than can be documented from phenotypic variation alone. Similarly, dominance of a single parental phenotype following an introduction event may lead to instances of species erosion being mistaken for species displacement without hybridization.
... The senior author of the Andrés et al. (2013) study, Richard G. Harrison, began investigating speciation in crickets in the mid-1970s using protein electrophoresis techniques. Since then, he and his colleagues have examined properties of cricket mitochondrial DNA (Harrison et al. 1985; Harrison 1986, 1989), studied hybrid zones where different species of crickets meet (Willett et al. 1997; Ross and Harrison 2002; Maroja et al. 2009), and investigated whether the bacterial parasite Wolbachia (Mandel et al. 2001; Maroja et al. 2008 ) and divergent reproductive proteins (Andrés et al. 2006Andrés et al. , 2008) contribute to speciation in crickets. Most recently, their studies have focused on G. firmus and G. pennsylvanicus, a pair of closely related species of field cricket found in the eastern region of North America. ...
Article
Unlabelled: Understanding evidence for the genetic basis of reproductive isolation is imperative for supporting students' understanding of mechanisms of speciation in courses such as Genetics and Evolutionary Biology. An article by Andrés et al. in the February 2013 issue of GENETICS illustrates how advances in DNA sequencing are accelerating studies of population genetics in species with limited genetic and genomic resources. Andrés et al. use the latest sequencing technologies to systematically identify and characterize sites in the DNA that vary within, and have diverged between, species to explore speciation in crickets. This primer, coupled with that article, will help instructors introduce and reinforce important concepts in genetics and evolution while simultaneously introducing modern methodology in the undergraduate classroom. Related article in Genetics: Andrés, J. A., E. L. Larson, S. M. Bogdanowicz, and R. G. Harrison, 2013 Patterns of transcriptome divergence in the male accessory gland of two closely related species of field crickets. Genetics 193: 501-513.
... Genes functionally tied to reproductive isolation should prove reliable markers for species identity if they perform poorly in a heterospecific genetic background and selection within species reduces variation in a way that limits lineage sorting. Such genes may be marked by limited introgression across hybrid zones (Rieseberg et al. 1999;Carling and Brumfield 2009;Maroja et al. 2009) and strong allele sorting in regions of sympatry with close relatives (Geyer and Palumbi 2003), and their gene trees may trace the true species tree more closely than those of neutral markers (Ting et al. 2000;Palopoli et al. 1996). ...
Article
Reproductive proteins commonly show signs of rapid divergence driven by positive selection. The mechanisms driving these changes have remained ambiguous in part because interacting male and female proteins have rarely been examined. We isolate an egg protein the vitelline envelope receptor for lysin (VERL) from Tegula, a genus of free-spawning marine snails. Like VERL from abalone, Tegula VERL is a major component of the VE surrounding the egg, includes a conserved zona pellucida (ZP) domain at its C-terminus, and possesses a unique, negatively charged domain of about 150 amino acids implicated in interactions with the positively charged lysin. Unlike for abalone VERL, where this unique VERL domain occurs in a tandem array of 22 repeats, Tegula VERL has just one such domain. Interspecific comparisons show that both lysin and the VERL domain diverge via positive selection, whereas the ZP domain evolves neutrally. Rates of nonsynonymous substitution are correlated between lysin and the VERL domain, consistent with sexual antagonism, although lineage-specific effects, perhaps owing to different ecologies, may alter the relative evolutionary rates of sperm- and egg-borne proteins.
... Complex patterns of genetic variation are expected among recently diverged lineages, and these patterns may be governed by both stochastic and deterministic processes (e.g. Maroja et al. 2009). For example, neutral polymorphisms are expected to be shared among daughter populations as a simple consequence of the persistence of polymorphisms present in the ancestral population. ...
Article
In the early stages of reproductive isolation, genomic regions of reduced recombination are expected to show greater levels of differentiation, either because gene flow between species is reduced in these regions or because the effects of selection at linked sites within species are enhanced in these regions. Here, we study the patterns of DNA sequence variation at 27 autosomal loci among populations of Mus musculus musculus, M. m. domesticus, and M. m. castaneus, three subspecies of house mice with collinear genomes. We found that some loci exhibit considerable shared variation among subspecies, while others exhibit fixed differences. We used an isolation-with-gene-flow model to estimate divergence times and effective population sizes (N(e) ) and to disentangle ancestral variation from gene flow. Estimates of divergence time indicate that all three subspecies diverged from one another within a very short period of time approximately 350,000 years ago. Overall, N(e) for each subspecies was associated with the degree of genetic differentiation: M. m. musculus had the smallest N(e) and the greatest proportion of monophyletic gene genealogies, while M. m. castaneus had the largest N(e) and the smallest proportion of monophyletic gene genealogies. M. m. domesticus and M. m. musculus were more differentiated from each other than either were from M. m. castaneus, consistent with greater reproductive isolation between M. m. domesticus and M. m. musculus. F(ST) was significantly greater at loci experiencing low recombination rates compared to loci experiencing high recombination rates in comparisons between M. m. castaneus and M. m. musculus or M. m. domesticus. These results provide evidence that genomic regions with less recombination show greater differentiation, even in the absence of chromosomal rearrangements.
Article
Rapid range shifts are one of the most frequent responses to climate change in insect populations. Climate-induced range shifts can lead to the breakdown of isolation barriers, and thus, to an increase in hybridization and introgression. Long-term evolutionary consequences such as the formation of hybrid zones, introgression, speciation and extinction have been predicted as the result of climate-induced hybridization. Our review shows that there has been an increase in the number of published cases of climate-induced hybridization in insects; and that the formation of hybrid zones and introgression seems to be, at the moment, the most frequent outcomes. Although introgression is considered positive, since it increases species’ genetic diversity, in the long term it could lead to negative outcomes such as species fusion or genetic swamping.
Article
Much of what we know about speciation comes from detailed studies of well‐known model systems. Although there have been several important syntheses on speciation, few (if any) have explicitly compared speciation among major groups across the Tree of Life. Here, we synthesize and compare what is known about key aspects of speciation across taxa, including bacteria, protists, fungi, plants, and major animal groups. We focus on three main questions. Is allopatric speciation predominant across groups? How common is ecological divergence of sister species (a requirement for ecological speciation), and on what niche axes do species diverge in each group? What are the reproductive isolating barriers in each group? Our review suggests the following patterns. (i) Based on our survey and projected species numbers, the most frequent speciation process across the Tree of Life may be co‐speciation between endosymbiotic bacteria and their insect hosts. (ii) Allopatric speciation appears to be present in all major groups, and may be the most common mode in both animals and plants, based on non‐overlapping ranges of sister species. (iii) Full sympatry of sister species is also widespread, and may be more common in fungi than allopatry. (iv) Full sympatry of sister species is more common in some marine animals than in terrestrial and freshwater ones. (v) Ecological divergence of sister species is widespread in all groups, including ~70% of surveyed species pairs of plants and insects. (vi) Major axes of ecological divergence involve species interactions (e.g. host‐switching) and habitat divergence. (vii) Prezygotic isolation appears to be generally more widespread and important than postzygotic isolation. (viii) Rates of diversification (and presumably speciation) are strikingly different across groups, with the fastest rates in plants, and successively slower rates in animals, fungi, and protists, with the slowest rates in prokaryotes. Overall, our study represents an initial step towards understanding general patterns in speciation across all organisms.
Article
The subfamily Eneopterinae is known greatly for its diversified acoustic modalities and disjunct distribution. Within Eneopterinae, tribe Lebinthini is the most studied group, due to its highest species diversity (ca. 150 species in 12 genera), endemic distribution on the islands of Southeast Asia and of the South West Pacific, males’ ability to produce high‐frequency calling songs, and evolution of females’ vibrational response. To investigate the distribution pattern and diversification of acoustic and behavioral attributes in a larger frame, clear understanding of phylogenetic relationships within other tribes of Eneopterinae is vital. In this study, we focus on the tribe Xenogryllini, sister group of Lebinthini. Xenogryllini, as opposed to Lebinthini, is known by fewer species (11 species in two genera), distributed widely in continental Asia and Africa, and for producing low‐frequency calling songs. We describe a new genus Indigryllus with a new species of the tribe Xenogryllini, discovered from the southwest of India. We used eight molecular genetic markers to reconstruct the phylogenetic relationships. The resultant phylogenetic tree is used to compare and discuss distribution patterns and acoustic modalities between Lebinthini and Xenogryllini. Subfamily Eneopterinae is known for its diversified acoustic modalities and disjunct distribution. In this study, we focus on the tribe Xenogryllini, sister group of the most diversified tribe Lebinthini. Xenogryllini is known by fewer species, distributed widely in continental Asia and Africa. We describe a new genus Indigryllus with a new species of the tribe Xenogryllini, discovered from the southwest of India and reconstruct molecular phylogenetic relationships within the tribe based on eight DNA markers. We discuss the distribution pattern and acoustic modalities between tribes Lebinthini and Xenogryllini.
Article
The origin of biological diversity, via the formation of new species, can be inextricably linked to adaptation to the ecological environment. Specifically, ecological processes are central to the formation of new species when barriers to gene flow (reproductive isolation) evolve between populations as a result of ecologically based divergent natural selection. This process of 'ecological speciation' has seen a large body of focused research in the last ten-fifteen years, and a review and synthesis of the theoretical and empirical literature is now timely. The book begins by clarifying what ecological speciation is, its alternatives, and the predictions that can be used to test for it. It then reviews the three components of ecological speciation and discusses the geography and genomic basis of the process. A final chapter highlights future research directions, describing the approaches and experiments which might be used to conduct that future work. The ecological and genetic literature is integrated throughout the text with the goal of shedding new insight into the speciation process, particularly when the empirical data is then further integrated with theory.
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Thesis
My dissertation addressed questions of the origin and maintenance of biodiversity, and the genomic response to environmental change in blue mussels (genus Mytilus). In chapters One and Two I explored the nature of species barriers and the consequence of hybridization. The ecological and genetic factors determining the extent of introgression between species in secondary contact zones remain poorly understood. I investigated the relative importance of natural selection and the demographic expansion of invasive Mytilus galloprovincialis on the magnitude and the direction of introgression with the native M. trossulus in a hybrid zone in central California. I used double-digest restriction-site associated DNA sequencing (ddRADseq) to genotype 1,751 randomly-selected single nucleotide polymorphisms and accurately distinguish early and advanced generation hybrids for the first time in Mytilus. I found that ecologically based selection plays only a small direct role in maintaining reproductive isolation in the California hybrid zone, and that colonization history is an important control on the movement of genetic elements (i.e. introgression) during hybridization. Despite only low rates of hybridization between invasive Mediterranean blue mussel (M. galloprovincialis) and native blue mussel M. trossulus, introgression is occurring, and the geographic spread of M. galloprovincialis appears to drive the majority of introgression into the invasive species. My work reinforces the idea that demographic processes mediate the role played by natural selection in maintaining species barriers. Chapter Three focused on the genetic consequences of large-scale environmental change. I developed new techniques using mRNA sequencing and ancestral state reconstruction to estimate rates of structurally stabilizing substitutions in blue mussels. I found that warm-adapted Mytilus galloprovincialis have higher rates of stabilizing substitutions than cold-adapted M. trossulus, which suggests that natural selection can efficiently modify structural properties of proteins to fine-tune thermal tolerance based on small changes in temperature of just several ̊C. As a whole, my dissertation reiterates the importance of demographic processes in controlling the movement of genetic material during hybridization, indicates introgression may contribute to invasive success, and documents subtle natural selection for changes in protein properties of warm adapted M. galloprovincialis.
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Before the establishment of reproductive isolation, deeply diverged intraspecific lineages can experience complex genetic and behavioral interactions as they come into secondary contact. Divergent selective and demographic processes mediate gene flow among lineages, resulting in hybrid zones with complex biogeographic structure. Discordance in the biogeographic patterns of autosomal and maternally inherited loci provides a useful window to infer the processes mediating admixture and introgression across hybrid zones. Here, we sampled 489 genotypes across a hybrid zone between 2 phylogeographic lineages of the spotted salamander, Ambystoma maculatum, and characterize discordant patterns of nuclear and mitochondrial introgression across the contact boundary. Our results indicate asymmetric introgression of nuclear DNA beyond the contact boundary from the western to eastern lineage, with introgression of eastern mitochondrial DNA into the western lineage. We discuss alternative mechanisms for this pattern and attribute this result to neutral patterns of population expansion of the western lineage into the east in combination with female mate choice for larger-bodied western males. Our results underscore the complexity of interacting mechanisms that give rise to reproductive asymmetries in the earliest stages of the speciation process. © The American Genetic Association 2015. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
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Comprising 50%-75% of the world's fauna, insects are a prominent part of biodiversity in communities and ecosystems globally. Biodiversity across all levels of biological classifications is fundamentally based on genetic diversity. However, the integration of genomics and phylogenetics into conservation management may not be as rapid as climate change. The genetics of hybrid introgression as a source of novel variation for ecological divergence and evolutionary speciation (and resilience) may generate adaptive potential and diversity fast enough to respond to locally-altered environmental conditions. Major plant and herbivore hybrid zones with associated communities deserve conservation consideration. This review addresses functional genetics across multi-trophic-level interactions including "invasive species" in various ecosystems as they may become disrupted in different ways by rapid climate change. "Invasive genes" (into new species and populations) need to be recognized for their positive creative potential and addressed in conservation programs. "Genetic rescue" via hybrid translocations may provide needed adaptive flexibility for rapid adaptation to environmental change. While concerns persist for some conservationists, this review emphasizes the positive aspects of hybrids and hybridization. Specific implications of natural genetic introgression are addressed with a few examples from butterflies, including transgressive phenotypes and climate-driven homoploid recombinant hybrid speciation. Some specific examples illustrate these points using the swallowtail butterflies (Papilionidae) with their long-term historical data base (phylogeographical diversity changes) and recent (3-decade) climate-driven temporal and genetic divergence in recombinant homoploid hybrids and relatively recent hybrid speciation of Papilio appalachiensis in North America. Climate-induced "reshuffling" (recombinations) of species composition, genotypes, and genomes may become increasingly ecologically and evolutionarily predictable, but future conservation management programs are more likely to remain constrained by human behavior than by lack of academic knowledge.
Article
Many marine ecologists aspire to use genetic data to understand how selection and demographic history shape the evolution of diverging populations as they become reproductively isolated species. I propose combining two types of genetic analysis focused on this key early stage of the speciation process to identify the selective agents directly responsible for population divergence. Isolation-with-migration (IM) models can be used to characterize reproductive isolation between populations (low gene flow), while codon models can be used to characterize selection for population differences at the molecular level (especially positive selection for high rates of amino acid substitution). Accessible transcriptome sequencing methods can generate the large quantities of data needed for both types of analysis. I highlight recent examples (including our work on fertilization genes in sea stars) in which this confluence of interest, models, and data has led to taxonomically broad advances in understanding marine speciation at the molecular level. I also highlight new models that incorporate both demography and selection: simulations based on these theoretical advances suggest that polymorphisms shared among individuals (a key source of information in IM models) may lead to false-positive evidence of selection (in codon models), especially during the early stages of population divergence and speciation that are most in need of study. The false-positive problem may be resolved through a combination of model improvements plus experiments that document the phenotypic and fitness effects of specific polymorphisms for which codon models and IM models indicate selection and reproductive isolation (such as genes that mediate sperm-egg compatibility at fertilization). © 2014 Marine Biological Laboratory.
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The study of speciation is concerned with understanding the connection between causes of divergent evolution and the origin and maintenance of barriers to gene exchange between incipient species. Although the field has historically focused either on examples of recent divergence and its causes or on the genetic basis of reproductive isolation between already divergent species, current efforts seek to unify these two approaches. Here we integrate these perspectives through a discussion of recent progress in several insect speciation model systems. We focus on the evolution of speciation phenotypes in each system (i.e., those phenotypes causally involved in reducing gene flow between incipient species), drawing an explicit connection between cause and effect (process and pattern). We emphasize emerging insights into the genomic architecture of speciation as well as timely areas for future research. Expected final online publication date for the Annual Review of Entomology Volume 59 is January 07, 2014. Please see http://www.annualreviews.org/catalog/pubdates.aspx for revised estimates.
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Reproductive barriers reduce gene flow between populations and maintain species identities. A diversity of barriers exist, acting before, during and after mating. To understand speciation and coexistence, these barriers need to be quantified and their potential interactions revealed. We use the hybridising field crickets Gryllus bimaculatus and G. campestris as a model to understand the full compliment and relative strength of reproductive barriers. We find that males of both species prefer conspecific females, but the effect is probably too weak to represent a barrier. In contrast, prezygotic barriers caused by females being more attracted to conspecific male song and preferentially mounting and mating with conspecifics are strong and asymmetric. Postzygotic barriers vary in direction; reductions in fecundity and egg viability create selection against hybridisation, but hybrids live longer than pure-bred individuals. Hybrid females show a strong preference for G. bimaculatus songs, which together with a complete lack of hybridisation by G. campestris females, suggests that asymmetric gene flow is likely. For comparison, we review reproductive barriers that have been identified between other Gryllids and conclude that multiple barriers are common. Different species pairs are separated by qualitatively different combinations of barriers, suggesting that reproductive isolation and even the process of speciation itself may vary widely even within closely related groups.
Article
Genealogical discordance, or when different genes tell distinct stories although they evolved under a shared history, often emerges from either coalescent stochasticity or introgression. In this study, we present a strong case of mito-nuclear genealogical discordance in the Australian rainforest lizard species complex of Saproscincus basiliscus and S. lewisi. One of the lineages that comprises this complex, the Southern S. basiliscus lineage, is deeply divergent at the mitochondrial genome but shows markedly less divergence at the nuclear genome. By placing our results in a comparative context and reconstructing the lineages' demography via multilocus and coalescent-based approximate Bayesian computation methods, we test hypotheses for how coalescent variance and introgression contribute to this pattern. These analyses suggest that the observed genealogical discordance likely results from introgression. Further, to generate such strong discordance, introgression probably acted in concert with other factors promoting asymmetric gene flow between the mitochondrial and nuclear genomes, such as selection or sex-biased dispersal. This study offers a framework for testing sources of genealogical discordance and suggests that historical introgression can be an important force shaping the genetic diversity of species and their populations.
Article
The origins of hybrid zones between parapatric taxa have been of particular interest for understanding the evolution of reproductive isolation and the geographic context of species divergence. One challenge has been to distinguish between allopatric divergence (followed by secondary contact) versus primary intergradation (parapatric speciation) as alternative divergence histories. Here, we use complementary phylogeographic and population genetic analyses to investigate the recent divergence of two subspecies of Clarkia xantiana and the formation of a hybrid zone within the narrow region of sympatry. We tested alternative phylogeographic models of divergence using approximate Bayesian computation (ABC) and found strong support for a secondary contact model and little support for a model allowing for gene flow throughout the divergence process (i.e. primary intergradation). Two independent methods for inferring the ancestral geography of each subspecies, one based on probabilistic character state reconstructions and the other on palaeo-distribution modelling, also support a model of divergence in allopatry and range expansion leading to secondary contact. The membership of individuals to genetic clusters suggests geographic substructure within each taxon where allopatric and sympatric samples are primarily found in separate clusters. We also observed coincidence and concordance of genetic clines across three types of molecular markers, which suggests that there is a strong barrier to gene flow. Taken together, our results provide evidence for allopatric divergence followed by range expansion leading to secondary contact. The location of refugial populations and the directionality of range expansion are consistent with expectations based on climate change since the last glacial maximum. Our approach also illustrates the utility of combining phylogeographic hypothesis testing with species distribution modelling and fine-scale population genetic analyses for inferring the geography of the divergence process.
Article
Abstract  With recent climate warming trends, both the increase in thermal variance (i.e., diurnal temperature range; DTR) as well as increased mean temperature may impact many different organisms, especially poikilothermic invertebrates. Predictions of insect developmental rates using degree-days (thermal unit accumulations above the developmental base threshold of the insect) are based on daily mean temperatures, regardless of DTR. However, non-linearity and variance in the means and extremes are often ignored. The role of thermal variance (e.g., daily temperature extremes and DTR) was evaluated experimentally for two swallowtail butterfly sister species using a common day/night photoperiod of 18: 6 h photo: scoto-phase and corresponding daytime thermophase and nighttime cryophase periods of 22: 22°C (constant 22°C), 24: 16°C, and 26: 10°C (all three treatments had the same daily mean and the same degree-day accumulations). Although developmental rates of post-diapause pupae were largely unaffected for both species, our results show that sizes in P. canadensis females (but not males) were smaller in the treatments with more variance (26°C: 10°C) compared to constant 22°C. Such potentially significant impacts of size reduction in P. canadensis females were not observed in P. glaucus males or females under the same series of thermo-period treatments.
Chapter
A hybrid zone occurs where two distinct genetic forms meet, mate and produce offspring with mixed genomes. Such zones may vary in width, length and patchiness, and are found between species, subspecies, races or forms. Stable hybrid zones may be maintained by selection against hybrids, environmental selection, or a combination of the two. A hybrid zone can arise either by direct environmental selection in contiguous populations or by renewed contact between previously isolated populations. Hybrid zones act as semi-permeable barriers, which allow gene exchange for neutral or adaptive characters, whereas restricting introgression of alleles that contribute to local adaptation or reduced hybrid fitness. The study of genomic regions that experience barriers to gene flow can provide an important window for identifying specific genes and mutations that underlie reproductive isolation and local adaptation. With the help of recent technological advances in development of thousands of molecular markers, distributed genome-wide, identification of such genomic regions is becoming possible in natural hybrid zones.
Article
Abstract The search for pattern in the ecology and evolutionary biology of insect–plant associations has fascinated biologists for centuries. High levels of tropical (low-latitude) plant and insect diversity relative to poleward latitudes and the disproportionate abundance of host-specialized insect herbivores have been noted. This review addresses several aspects of local insect specialization, host use abilities (and loss of these abilities with specialization), host-associated evolutionary divergence, and ecological (including “hybrid”) speciation, with special reference to the generation of biodiversity and the geographic and taxonomic identification of “species borders” for swallowtail butterflies (Papilionidae). From ancient phytochemically defined angiosperm affiliations that trace back millions of years to recent and very local specialized populations, the Papilionidae (swallowtail butterflies) have provided a model for enhanced understanding of localized ecological patterns and genetically based evolutionary processes. They have served as a useful group for evaluating the feeding specialization/physiological efficiency hypothesis. They have shown how the abiotic (thermal) environment interacts with host nutrirional suitability to generate “voltinism/suitability” gradients in specialization or preference latitudinally, and geographical mosaics locally. Several studies reviewed here suggest strongly that the oscillation hypothesis for speciation does have considerable merit, but at the same time, some species-level host specializations may lead to evolutionary dead-ends, especially with rapid environmental/habitat changes involving their host plants. Latitudinal gradients in species richness and degree of herbivore feeding specialization have been impacted by recent developments in ecological genetics and evolutionary ecology. Localized insect–plant associations that span the biospectrum from polyphenisms, polymorphisms, biotypes, demes, host races, to cryptic species, remain academically contentious, with simple definitions still debated. However, molecular analyses combined with ecological, ethological and physiological studies, have already begun to unveil some answers for many important ecological/evolutionary questions.
Article
Abstract The ecology and evolutionary biology of insect–plant associations has realized extensive attention, especially during the past 60 years. The classifications (categorical designations) of continuous variation in biodiversity, ranging from global patterns (e.g., latitudinal gradients in species richness/diversity and degree of herbivore feeding specialization) to localized insect–plant associations that span the biospectrum from polyphenisms, polymorphisms, biotypes, demes, host races, to cryptic species, remain academically contentious. Semantic and biosystematic (taxonomical) disagreements sometimes detract from more important ecological and evolutionary processes that drive diversification, the dynamics of gene flow and local extinctions. This review addresses several aspects of insect specialization, host-associated divergence and ecological (including “hybrid”) speciation, with special reference to the climate warming impacts on species borders of hybridizing swallowtail butterflies (Papilionidae). Interspecific hybrid introgression may result in collapse of multi-species communities or increase species numbers via homoploid hybrid speciation. We may see diverging, merging, or emerging genotypes across hybrid zones, all part of the ongoing processes of evolution. Molecular analyses of genetic mosaics and genomic dynamics with “divergence hitchhiking”, combined with ecological, ethological and physiological studies of “species porosity”, have already begun to unveil some answers for some important ecological/evolutionary questions. (i) How rapidly can host-associated divergence lead to new species (and why doesn't it always do so, e.g., resulting in “incomplete” speciation)? (ii) How might “speciation genes” function, and how/where would we find them? (iii) Can oscillations from specialists to generalists and back to specialists help explain global diversity in herbivorous insects? (iv) How could recombinant interspecific hybridization lead to divergence and speciation? From ancient phytochemically defined angiosperm affiliations to recent and very local geographical mosaics, the Papilionidae (swallowtail butterflies) have provided a model for enhanced understanding of ecological patterns and evolutionary processes, including host-associated genetic divergence, genomic mosaics, genetic hitchhiking and sex-linked speciation genes. Apparent homoploid hybrid speciation in Papilio appears to have been catalyzed by climate warming-induced interspecific introgression of some, but not all, species diagnostic traits, reflecting strong divergent selection (discordant), especially on the Z (= X) chromosome. Reproductive isolation of these novel recombinant hybrid genotypes appears to be accomplished via a delayed post-diapause emergence or temporal isolation, and is perhaps aided by the thermal landscape. Changing thermal landscapes appear to have created (and may destroy) novel recombinant hybrid genotypes and hybrid species.
Article
Long neglected by classic island biogeographical theory, speciation within and among islands is increasingly recognized as a major contributor to insular diversity. Although the factors responsible for island speciation remain poorly understood, this process appears critically dependent on geographical variation and speciation in allopatry or parapatry. Here, we investigate geographical variation and speciation in a complex of Hispaniolan trunk anoles (Anolis distichus), where populations with strikingly distinct dewlap colours and patterns correspond with deeply divergent mtDNA structure. Using a multilocus, population-level analysis, we investigate whether these phenotypically and mitochondrially distinct populations exhibit the type of nuclear differentiation expected among species or incipient species. Along a transect that extends across a recently recessed marine barrier, our results are consistent with the persistence of an abrupt phenotypic and mitochondrial transition following secondary contact, in spite of little or no evidence for a reduction in nuclear gene flow. Along a second transect extending across a steep environmental gradient, our phenotypic and microsatellite data suggest a sharp genetic break with little or no admixture, whereas mtDNA recovers a signature of extensive unidirectional introgression. Together, these results are consistent with previous studies of Lesser Antillean anoles, suggesting that allopatric divergence alone is insufficient for speciation, whereas reduced gene flow and partial reproductive isolation may accumulate in the presence of ecological gradients.
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The pattern of character variation within a hybrid zone, the hybrid zone structure, has been used to infer the processes that maintain hybrid zones. Unfortunately it is difficult to infer process from structure alone because many different processes can produce the same pattern of character variation. Mosaic hybrid zones may be maintained by exogenous selection in a heterogeneous environment and/or endogenous selection against hybrid individuals: habitat preference, premating isolating barriers and/or fertility selection can also contribute. The spatial scale at which a hybrid zone is sampled affects its apparent structured a hybrid zone may appear clinal at one scale and mosaic at another. Here, we sample the mosaic hybrid zone between two field crickets, Gryllus firmus and G. pennsylvanicus, at a scale that spans the boundaries between individual soil-habitat patches. From our analysis, we find that at fine scales, the mosaic hybrid zone resolves into a set of steep clines across patch boundaries. Both morphological and molecular traits exhibit sharp and generally concordant clines. However, clines for mitochondrial DNA and one anonymous nuclear marker are clearly displaced as a result of current hybridization or past introregression (the "ghost of hybridization past"). Thus, scale is important for the structure of this and probably other hybrid zones. The extremely sharp, concordant clines across patch boundaries indicate that the cricket hybrid zone is undoubtedly structured by selection. However, the detailed mechanisms responsible for the maintenance of the hybrid zone-whether endogenous selection against hybrids, exogenous selection by the environment, and/or behavioral preferences for mates or habitats remain to be elucidated. Determining these mechanisms will depend on closer inspection of the organisms themselves and their interactions, as is the case for all hybrid zones.
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An official journal of the Genetics Society, Heredity publishes high-quality articles describing original research and theoretical insights in all areas of genetics. Research papers are complimented by News & Commentary articles and reviews, keeping researchers and students abreast of hot topics in the field.
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The divergence of Drosophila pseudoobscura from its close relatives, D. persimilis and D. pseudoobscura bogotana, was examined using the pattern of DNA sequence variation in a common set of 50 inbred lines at 11 loci from diverse locations in the genome. Drosophila pseudoobscura and D. persimilis show a marked excess of low-frequency variation across loci, consistent with a model of recent population expansion in both species. The different loci vary considerably, both in polymorphism levels and in the levels of polymorphisms that are shared by different species pairs. A major question we address is whether these patterns of shared variation are best explained by gene flow or by persistence since common ancestry. A new test of gene flow, based on patterns of linkage disequilibrium, is developed. The results from these, and other tests, support a model in which D. pseudoobscura and D. persimilis have exchanged genes at some loci. However, the pattern of variation suggests that most gene flow, although occurring after speciation began, was not recent. There is less evidence of gene flow between D. pseudoobscura and D. p. bogotana. The results are compared with recent work on the genomic locations of genes that contribute to reproductive isolation between D. pseudoobscura and D. persimilis. We show that there is a good correspondence between the genomic regions associated with reproductive isolation and the regions that show little or no evidence of gene flow.
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We investigated the effects that habitat variation has on the structure and dynamics of a hybrid zone between two closely related crickets in Connecticut. A collecting protocol was developed in which crickets were sampled from characteristic habitats on either side of the hybrid zone and from two distinct habitat types within the zone. Presumptive pure Gryllus pennsylvanicus were sampled from fields in northwestern Connecticut and represent "inland" populations. "Pure" Gryllus firmus were sampled from beaches along the coast and represent the "coastal" populations. Crickets from within the hybrid zone were sampled from two different soil types: the "loam" populations from loamy soils and the "sand" populations from sandy soils. Moreover, an attempt was made to identify closely adjacent sand and loam localities to determine the scale of habitat variation and its possible effects on hybrid-zone structure. In general, there was little variation in morphological traits or in allozyme and mtDNA genotype frequencies among localities from within each of the four habitat types. Between each of the closely situated sand and loam localities within the hybrid zone, however, there were very significant differences in each of these sets of markers. In addition, crickets from hybrid-zone populations were tested for reproductive isolation. The asymmetric outcome of hybrid crosses that exists across the zone (Harrison, 1983) also exists on a finer ecological scale within the zone. Thus, this hybrid zone is a mosaic of strikingly differentiated populations. The dynamics of hybrid zones with mosaic structures are discussed in contrast to the traditional clinal models. The data are also discussed in light of the semipermeable nature of species boundaries. The extent to which a species boundary is permeable varies not only from one genetic marker to the next, but also with the ecological and geographic context of species interaction.
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ROGERS, DS, IF GREENBAUM, SJ GUNN, AND MD ENGSTROM. 1984. Cytosystematic value of chromosomal inversion data in the genus Peromyscus (Rodentia: Cricetidae). J. Mammal. 65: 457-465. RUVOLO, M. 1992. Molecular evolutionary processes can produce ...
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Habitat segregation allows recently diverged taxa to minimize competition and maximize fitness. Consequently, the overall distribution of a species in part will be determined by interactions with their close relatives. Two recently diverged but hybridizing field crickets, Gryllus firmus and G. pennsylvanicus, form a mosaic hybrid zone in Connecticut in which each species is associated with a specific soil type: G. firmus is found on sand soils and G. pennsylvanicus is found on loam soils. Both species produce diapausing eggs, which spend the winter in the ground. We investigate how viability selection on overwintering eggs in different soils influences the distributions of the two species, habitat partitioning between them, and the structure of the mosaic hybrid zone. Our results suggest that selection on eggs by soil types is not important in determining the success of crickets on different soils. However, winter climate has a strong effect on egg viability, and variation in egg survivorship over different winter climate regimes likely plays an important role in determining the distribution of these cricket species and the position of the hybrid zone.
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The relationship between species is usually represented as a bifurcating tree with the branching points representing speciation events. The ancestry of genes taken from these species can also be represented as a tree, with the branching points representing ancestral genes. The time back to the branching points, and even the branching order, can be different between the two trees. This possibility is widely recognized, but the discrepancies are often thought to be small. A different picture is emerging from new empirical evidence, particularly that based on multiple loci or on surveys with a wide geographical scope. The discrepancies must be taken into account when estimating the timing of speciation events, especially the more recent branches. On the positive side, the different timings at different loci provide information about the ancestral populations.
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The program MRBAYES performs Bayesian inference of phylogeny using a variant of Markov chain Monte Carlo. Availability: MRBAYES, including the source code, documentation, sample data files, and an executable, is available at http://brahms.biology.rochester.edu/software.html. Contact: johnh{at}brahms.biology.rochester.edu
Article
We introduce a new statistical model for patterns of linkage disequilibrium (LD) among multiple SNPs in a population sample. The model overcomes limitations of existing approaches to understanding, summarizing, and interpreting LD by (i) relating patterns of LD directly to the underlying recombination process; (ii) considering all loci simultaneously, rather than pairwise; (iii) avoiding the assumption that LD necessarily has a “block-like” structure; and (iv) being computationally tractable for huge genomic regions (up to complete chromosomes). We examine in detail one natural application of the model: estimation of underlying recombination rates from population data. Using simulation, we show that in the case where recombination is assumed constant across the region of interest, recombination rate estimates based on our model are competitive with the very best of current available methods. More importantly, we demonstrate, on real and simulated data, the potential of the model to help identify and quantify fine-scale variation in recombination rate from population data. We also outline how the model could be useful in other contexts, such as in the development of more efficient haplotype-based methods for LD mapping.
Article
The seminal fluid that is transferred along with sperm during mating acts in many ways to maximize a male’s reproductive success. Here, we use transgenic Drosophila melanogaster males deficient in the seminal fluid proteins derived from the accessory gland (Acps) to investigate the role of these proteins in the fate of sperm transferred to females during mating. Competitive PCR assays were used to show that while Acps contribute to the efficiency of sperm transfer, they are not essential for the transfer of sperm to the female. In contrast, we found that Acps are essential for storage of sperm by females. Direct counts of stored sperm showed that 10% of normal levels are stored by females whose mates transfer little or no Acps along with sperm.
Article
Genetic analyses of reproductive barriers represent one of the few methods by which theories of speciation can be tested. However, genetic study is often restricted to model organisms that have short generation times and are easily propagated in the laboratory. Replicate hybrid zones with a diversity of recombinant genotypes of varying age offer increased resolution for genetic mapping experiments and expand the pool of organisms amenable to genetic study. Using 88 markers distributed across 17 chromosomes, we analyze the introgression of chromosomal segments of Helianthus petiolaris into H. annuus in three natural hybrid zones. Introgression was significantly reduced relative to neutral expectations for 26 chromosomal segments, suggesting that each segment contains one or more factors that contribute to isolation. Pollen sterility is significantly associated with 16 of these 26 segments, providing a straightforward explanation of why this subset of blocks is disadvantageous in hybrids. In addition, comparison of rates of introgression across colinear vs. rearranged chromosomes indicates that close to 50% of the barrier to introgression is due to chromosomal rearrangements. These results demonstrate the utility of hybrid zones for identifying factors contributing to isolation and verify the prediction of increased resolution relative to controlled crosses.
Article
Mated females of many animal species store sperm. Sperm storage profoundly influences the number, timing, and paternity of the female’s progeny. To investigate mechanisms for sperm storage in Drosophila melanogaster, we generated and analyzed mutations in Acp36DE. Acp36DE is a male seminal fluid protein whose localization in mated females suggested a role in sperm storage. We report that male-derived Acp36DE is essential for efficient sperm storage by females. Acp36DE1 (null) mutant males produced and transferred normal amounts of sperm and seminal fluid proteins. However, mates of Acp36DE1 males stored only 15% as many sperm and produced 10% as many adult progeny as control-mated females. Moreover, without Acp36DE, mated females failed to maintain an elevated egg-laying rate and decreased receptivity, behaviors whose persistence (but not initiation) normally depends on the presence of stored sperm. Previous studies suggested that a barrier in the oviduct confines sperm and Acp36DE to a limited area near the storage organs. We show that Acp36DE is not required for barrier formation, but both Acp36DE and the barrier are required for maximal sperm storage. Acp36DE associates tightly with sperm. Our results indicate that Acp36DE is essential for the initial storage of sperm, and that it may also influence the arrangement and retention of stored sperm.
Article
In this paper we show that when Drosophila melanogaster females are mated twice, the semen of the second male causes a reduction of the effective number of resident sperm from the previous mating. This is demonstrated by two different kinds of experiments. In one set of experiments, mated females were remated to two different kinds of sterile males, one with normal semen and the other with deficient semen. The effect on the resident sperm was determined from the number of remaining progeny after mating to the sterile male, with the result that the normal semen reduced the amount of resident sperm in comparison with matings to the males with deficient semen. The second set of experiments employed interrupted matings. These experiments were based on the observation that semen is delivered before sperm during the first 5 min of copulation. The second matings were interrupted instantly, 2 min, and 4 min after the initiation of copulation. Compared to the instant interruptions, the two later interruptions had the effect of reducing the amount of resident sperm. The results of these two experiments clearly indicate that a sperm-incapacitation process plays a role in the well-documented phenomenon of sperm displacement (last-male advantage) in this species. Such a process could play a role in sperm displacement in the many cases where the mechanism is unknown.
Article
We investigated the effects that habitat variation has on the structure and dynamics of a hybrid zone between two closely related crickets in Connecticut. A collecting protocol was developed in which crickets were sampled from characteristic habitats on either side of the hybrid zone and from two distinct habitat types within the zone. Presumptive pure Gryllus pennsylvanicus were sampled from fields in northwestern Connecticut and represent "inland" populations. "Pure" Gryllus firmus were sampled from beaches along the coast and represent the "coastal" populations. Crickets from within the hybrid zone were sampled from two different soil types: the "loam" populations from loamy soils and the "sand" populations from sandy soils. Moreover, an attempt was made to identify closely adjacent sand and loam localities to determine the scale of habitat variation and its possible effects on hybrid-zone structure. In general, there was little variation in morphological traits or in allozyme and mtDNA genotype frequencies among localities from within each of the four habitat types. Between each of the closely situated sand and loam localities within the hybrid zone, however, there were very significant differences in each of these sets of markers. In addition, crickets from hybrid-zone populations were tested for reproductive isolation. The asymmetric outcome of hybrid crosses that exists across the zone (Harrison, 1983) also exists on a finer ecological scale within the zone. Thus, this hybrid zone is a mosaic of strikingly differentiated populations. The dynamics of hybrid zones with mosaic structures are discussed in contrast to the traditional clinal models. The data are also discussed in light of the semipermeable nature of species boundaries. The extent to which a species boundary is permeable varies not only from one genetic marker to the next, but also with the ecological and geographic context of species interaction.
Article
Two closely related species of ground crickets, Allonemobius fasciatus and A. socius, overlap and hybridize in a contact zone in the eastern United States. In earlier work, Howard (1986) described geographic variation in the width of the zone and in the strength of reproductive isolation between the two ground crickets. The zone was wider in the hills and mountains of southeastern Ohio and West Virginia than along the eastern coastal plain, and reproductive isolation appeared to be stronger where the zone was wider. Howard attributed the greater width in the mountains to the wide intermingling and patchy distribution of habitats appropriate for a species adapted to a northern climate and for a species adapted to a southern climate. He also pointed out that the mosaicism and the increased breadth of the zone in the mountains enhanced the probability of occurrence of reinforcement. We tested three predictions that emerged from Howard's hypothesized links among topographic diversity, zone width, and the strength of reproductive isolation. The first two predictions were fulfilled. The northern cricket, A. fasciatus, occurred in the high mountains south of its previously known distributional limit; and the zone narrowed considerably in Illinois, an area of low topographic diversity. These results provide further evidence for the importance of the environment in determining the structure of the zone. The third prediction was falsified. Contrary to the prediction, the strength of reproductive isolation between the two species was as strong in Illinois as in the Appalachian Mountains. This result suggests that if reinforcement has occurred in the zone, the width of the zone has not been a major factor in the process.
Article
The distribution of multilocus genotypes found within a natural hybrid zone is determined by the sample of genotypes present when the hybrid zone first formed, by subsequent patterns of genetic exchange between the hybridizing taxa, and by drift and selection within each of the hybrid zone populations. We have used anonymous nuclear DNA restriction fragment polymorphisms (RFLPs) to characterize the array of multilocus genotypes present within a well-studied hybrid zone between two eastern North American field crickets, Gryllus pennsylvanicus and Gryllus firmus. These crickets hybridize along a zone of contact that extends from New England to Virginia. Previous studies have shown that both premating and postmating barriers exist between the two cricket species, but the absence of diagnostic morphological and allozyme markers has made it difficult to assess the consequences of these barriers for genetic exchange. Analyses based on four diagnostic anonymous nuclear markers indicate that hybrid zone populations in Connecticut contain few F1 hybrids, and that nonrandom associations persist among nuclear gene markers, between nuclear and cytoplasmic markers, and between molecular markers and morphology. Field cricket populations within the hybrid zone are not "hybrid swarms" but consist primarily of crickets that are very much like one or the other of the parental species. Despite ample opportunity for genetic exchange and evidence for introgression at some loci, the two species remain quite distinct. Such a pattern appears to be characteristic of many natural hybrid zones.
Article
The closely related field crickets Gryllus firmus and Gryllus pennsylvanicus are known to hybridize in a zone of contact that extends over more than 800 km from the Blue Ridge in Virginia to southern Connecticut. Here I present evidence that the extent of temporal reproductive isolation of the two cricket species varies along the length of the zone. Adults of G. firmus and G. pennsylvanicus occur synchronously in Connecticut but G. firmus matures significantly later than G. pennsylvanicus along the Blue Ridge in Virginia. Variation in the extent of temporal isolation is a consequence of intrinsic differences in the egg-to-adult development time of G. firmus from the two localities. In laboratory rearing experiments, there is little variation in development time among crickets from G. pennsylvanicus populations ranging from Vermont to Virginia. However, G. firmus from Virginia takes significantly longer to mature than G. firmus from Connecticut. Comparisons between species from neighboring localities show that lowland Virginia G. firmus take much longer to develop and are larger as adults than montane Virginia G. pennsylvanicus. In Connecticut, crickets of the two species differ very little in development time and body size. Patterns of variation in development time and body size are compared with similar data for frogs along one of the same environmental gradients and for field crickets along similar gradients elsewhere. Although G. firmus and G. pennsylvanicus are temporally isolated in Virginia, adults of the two species do occur together. Examination of Esterase genotypes of field-inseminated females and their progeny from a mixed population on the Blue Ridge suggests that pre-mating barriers other than temporal isolation are not effective in preventing gene exchange.
Chapter
Systematists and population geneticists can both use molecular data sets to construct evolutionary trees (species and gene trees, respectively), and then use the resulting historical framework to test a variety of hypotheses. The greatest prospect for future advances in our understanding of speciation is to extend these historical approaches to the species/population interface, for only by straddling this interface can we actually study the processes involved in the origin of a new species. This chapter illustrates how the bottomup historical approaches used in population genetics can be extended upward to this critical interface in order to separate the effects of population structure from population history, to rigorously test the species status of a group and to test hypotheses about the process of speciation by using gene trees to define a nested, statistical analysis of biogeographic and other types of data.
Chapter
Current gene tree models, developed and used by population geneticists for research on natural selection, can also be used to ask questions about the formation of species. When these gene tree models are joined with a null model of speciation, a research plan emerges that shows promise of revealing the extent to which genetic variation between populations contributes to the formation of species. The empirical element of this research plan requires that multiple DNA sequences be collected from each of the species investigated, and that these data come from multiple loci. Examples of these models and their application to recent data on the Drosophila melanogaster species complex are given.
Article
The divergence of Drosophila pseudoobscura and close relatives D. persimilis and D. pseudoobscura bogotana has been studied using comparative DNA sequence data from multiple nuclear loci. New data from the Hsp82 and Adh regions, in conjunction with existing data from Adh and the Period locus, are examined in the light of various models of speciation. The principal finding is that the three loci present very different histories, with Adh indicating large amounts of recent gene flow among the taxa, while little or no gene flow is apparent in the data from the other loci. The data were compared with predictions from several isolation models of divergence. These models include no gene flow, and they were found to be incompatible with the data. Instead the DNA data, taken together with other evidence, seem consistent with divergence models in which natural selection acts against gene flow at some loci more than at others. This family of models includes some sympatric and parapatric speciation models, as well as models of secondary contact and subsequent reinforcement of sexual isolation.
Article
The homeodomain is a DNA binding motif that is usually conserved among diverse taxa. Rapidly evolving homeodomains are thus of interest because their divergence may be associated with speciation. The exact site of the Odysseus (Ods) locus of hybrid male sterility inDrosophila contains such a homeobox gene. In the past half million years, this homeodomain has experienced more amino acid substitutions than it did in the preceding 700 million years; during this period, it has also evolved faster than other parts of the protein or even the introns. Such rapid sequence divergence is driven by positive selection and may contribute to reproductive isolation.
Article
There is still considerable uncertainty about the distributional and evolutionary relationships of the closely related North American field crickets, Gryllus pennsylvanicus and G. firmus. Although the two species differ in morphology and electromorph frequency, no single character is diagnostic. Here we present data on morphological and allozymic variation in 51 collections of fall adult field crickets from the eastern United States. It is clear from these data that two forms of fall adult crickets occur in the northeastern United States. One of the two forms, found primarily in inland or upland localities, is G. pennsylvanicus. A coastal/lowland form is similar in all respects to G. firmus from the southeastern United States. We suggest that the range of G. firmus extends considerably further north and inland than has previously been reported. Our data reveal an extensive zone of interaction between G. pennsylvanicus and G. firmus in the eastern United States. This zone appears to follow the eastern-most ridge of mountains (the Blue Ridge in Virginia, the Appalachians in Pennsylvania, New Jersey and New York). Observations of morphology and Est genotypes of individual crickets from mixed or intermediate populations suggest that little gene exchange occurs where the species are found together in Virginia. However, significant gene exchange may occur in areas of the northeast. Possible origins for the current distributions of G. pennsylvanicus and G. firmus are discussed.
Article
The closely related field crickets Gryllus firmus and Gryllus pennsylvanicus are known to hybridize in a zone of contact that extends over more than 800 km from the Blue Ridge in Virginia to southern Connecticut. Here I present evidence that the extent of temporal reproductive isolation of the two cricket species varies along the length of the zone. Adults of G. firmus and G. pennsylvanicus occur synchronously in Connecticut but G. firmus matures significantly later than G. pennsylvanicus along the Blue Ridge in Virginia. Variation in the extent of temporal isolation is a consequence of intrinsic differences in the egg-to-adult development time of G. firmus from the two localities. In laboratory rearing experiments, there is little variation in development time among crickets from G. pennsylvanicus populations ranging from Vermont to Virginia. However, G. firmus from Virginia takes significantly longer to mature than G. firmus from Connecticut. Comparisons between species from neighboring localities show that lowland Virginia G. firmus take much longer to develop and are larger as adults than montane Virginia G. pennsylvanicus. In Connecticut, crickets of the two species differ very little in development time and body size. Patterns of variation in development time and body size are compared with similar data for frogs along one of the same environmental gradients and for field crickets along similar gradients elsewhere. Although G. firmus and G. pennsylvanicus are temporally isolated in Virginia, adults of the two species do occur together. Examination of Esterase genotypes of field-inseminated females and their progeny from a mixed population on the Blue Ridge suggests that premating barriers other than temporal isolation are not effective in preventing gene exchange.
Article
In this paper we show that when Drosophila melanogaster females are mated twice, the semen of the second male causes a reduction of the effective number of resident sperm from the previous mating. This is demonstrated by two different kinds of experiments. In one set of experiments, mated females were remated to two different kinds of sterile males, one with normal semen and the other with deficient semen. The effect on the resident sperm was determined from the number of remaining progeny after mating to the sterile male, with the result that the normal semen reduced the amount of resident sperm in comparison with matings to the males with deficient semen. The second set of experiments employed interrupted matings. These experiments were based on the observation that semen is delivered before sperm during the first 5 min of copulation. The second matings were interrupted instantly, 2 min, and 4 min after the initiation of copulation. Compared to the instant interruptions, the two later interruptions had the effect of reducing the amount of resident sperm. The results of these two experiments clearly indicate that a spermincapacitation process plays a role in the well-documented phenomenon of sperm displacement (last-male advantage) in this species. Such a process could play a role in sperm displacement in the many cases where the mechanism is unknown.
Article
Two closely related species of ground crickets, Allonemobius fasciatus and A. socius, overlap and hybridize in a contact zone in the eastern United States. In earlier work, Howard (1986) described geographic variation in the width of the zone and in the strength of reproductive isolation between the two ground crickets. The zone was wider in the hills and mountains of southeastern Ohio and West Virginia than along the eastern coastal plain, and reproductive isolation appeared to be stronger where the zone was wider. Howard attributed the greater width in the mountains to the wide intermingling and patchy distribution of habitats appropriate for a species adapted to a northern climate and for a species adapted to a southern climate. He also pointed out that the mosaicism and the increased breadth of the zone in the mountains enhanced the probability of occurrence of reinforcement. We tested three predictions that emerged from Howard's hypothesized links among topographic diversity, zone width, and the strength of reproductive isolation. The first two predictions were fulfilled. The northern cricket, A. fasciatus, occurred in the high mountains south of its previously known distributional limit; and the zone narrowed considerably in Illinois, an area of low topographic diversity. These results provide further evidence for the importance of the environment in determining the structure of the zone. The third prediction was falsified. Contrary to the prediction, the strength of reproductive isolation between the two species was as strong in Illinois as in the Appalachian Mountains. This result suggests that if reinforcement has occurred in the zone, the width of the zone has not been a major factor in the process.
Article
The distribution of multilocus genotypes found within a natural hybrid zone is determined by the sample of genotypes present when the hybrid zone first formed, by subsequent patterns of genetic exchange between the hybridizing taxa, and by drift and selection within each of the hybrid zone populations. We have used anonymous nuclear DNA restriction fragment polymorphisms (RFLPs) to characterize the array of multilocus genotypes present within a well-studied hybrid zone between two eastern North American field crickets, Gryllus pennsylvanicus and Gryllus firmus. These crickets hybridize along a zone of contact that extends from New England to Virginia. Previous studies have shown that both premating and postmating barriers exist between the two cricket species, but the absence of diagnostic morphological and allozyme markers has made it difficult to assess the consequences of these barriers for genetic exchange. Analyses based on four diagnostic anonymous nuclear markers indicate that hybrid zone populations in Connecticut contain few F1 hybrids, and that nonrandom associations persist among nuclear gene markers, between nuclear and cytoplasmic markers, and between molecular markers and morphology. Field cricket populations within the hybrid zone are not 'hybrid swarms' but consist primarily of crickets that are very much like one or the other of the parental species. Despite ample opportunity for genetic exchange and evidence for introgression at some loci, the two species remain quite distinct. Such a pattern appears to be characteristic of many natural hybrid zones.
Article
Studies of field crickets (Orthoptera: Gryllidae) have emphasized the importance of life cycle evolution in the speciation process. Here I have used data from electrophoretic surveys of genetic variation in seven North American species of Gryllus to estimate genetic similarity between species. Relationships based on biochemical characters are significantly different from those previously established on the basis of morphology, song, distribution, and habitat. In particular, the sibling species Gryllus veletis and G pennsylvanicus appear to belong to distinct evolutionary lineages. Each is most closely related to other species with the same life cycle. These results do not lend support to the model of allochronic speciation (Alexander and Bigelow, 1960), which proposes that G veletis and G pennsylvanicus recently diverged through temporal isolation of previously interbreeding populations. Rather, it is suggested that each of the three diapausing life cycles characteristic of North American Gryllus may have had a unique and independent origin (perhaps from non-diapausing ancestors). If this is correct, the remarkable similarity between G veletis and G. pennsylvanicus in morphology and song must be explained in terms other than close phylogenetic relationship.
Article
The field crickets Gryllus pennsylvanicus and Gryllus firmus hybridize and/or overlap in a narrow zone that stretches from the Blue Ridge Mountains in Virginia to southern Connecticut. This paper examines post-mating barriers to gene exchange between the two cricket species. Field-collected crickets from two sets of paired localities were used in laboratory hybridization studies. The paired localities represent G pennsylvanicus and G. firmus populations adjacent to the zone of hybridization/overlap. Crosses between G pennsylvanicus males and G firmus females consistently failed to produce offspring. In contrast, the reciprocal cross resulted in viable and fertile F1 hybrids. The outcome was not dependent on the locality from which the parents were obtained. Observations of spermatophore transfer demonstrated that the failure of the G. pennsylvanicus male ×G. firmus female cross was indeed the result of a post-mating barrier. I evaluate the significance of these results for understanding both the origin of the hybrid zone and current patterns of gene exchange. I also consider possible explanations for the asymmetry in the outcome of the two reciprocal interspecific crosses.
Article
Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. C SIMON, F FRATI, A BECKENBACH, B CRESPI, H LIU, P
Article
The field cricket species, Gryllus firmusand G. pennsylvanicus,occur in a mosaic hybrid zone that roughly parallels the eastern slope of the Appalachian mountains in the northeastern United States. It is important to know what role, if any, the calling song plays in mate choice in sympatric and allopatric populations. In this report, we present results on the variability of calling song properties along transects across this hybrid zone. We also present the results of experiments on phonotactic selectivity of females from an allopatric population of G. firmus.The male calling song of allopatric G. firmuswas significantly slower in temporal rhythm (i. e., chirp and pulse repetition rates) and lower in pitch (i.e., dominant frequency) than that of allopatric G. pennsylvanicus.Calling song properties of males recorded in the hybrid zone varied considerably in temporal and spectral properties. In two-stimulus (choice) phonotaxis experiments, allopatric females of G. firmuspreferred synthetic calling songs with conspecific pulse repetition rates over songs that had lower and higher pulse rates. This preference persisted even when the sound pressure levels of alternative stimuli were unequal. Therefore, allopatric females of G. firmuscan discriminate between conspecific and heterospecific calling songs. Whether or not this same selectivity is present in sympatric populations remains unclear. Investigations of phonotactic selectivity in other allopatric and sympatric populations of both species are currently under way.