Interspecific competition, hybridization, and reproductive isolation in secondary contact: missing perspectives on males and females

We review the significance of two forms of sexual conflict (different evolutionary interests of the two sexes) for genetic differentiation of populations and the evolution of reproductive isolation. Conflicting selection on the alleles at a single locus can occur in males and females if the sexes have different optima for a trait, and there are pleiotropic genetic correlations between the sexes for it. There will then be selection for sex limitation and hence sexual dimorphism. This sex limitation could break down in hybrids and reduce their fitness. Pleiotropic genetic correlations between the sexes could also affect the likelihood of mating in interpopulation encounters. Conflict can also occur between (sex–limited) loci that determine behaviour in males and those that determine behaviour in females. Reproductive isolation may occur by rapid coevolution of male trait and female mating preference. This would tend to generate assortative mating on secondary contact, hence promoting speciation. Sexual conflict resulting from sensory exploitation, polyspermy and the cost of mating could result in high levels of interpopulation mating. If females evolve resistance to male pre– and postmating manipulation, males from one population could be more successful with females from the other, because females would have evolved resistance to their own (but not to the allopatric) males. Between–locus sexual conflict could also occur as a result of confict between males and females of different populations over the production of unfit hybrids. We develop models which show that females are in general selected to resist such matings and males to persist, and this could have a bearing on both the initial level of interpopulation matings and the likelihood that reinforcement will occur. In effect, selection on males usually acts to promote gene flow and to restrict premating isolation, whereas selection on females usually acts in the reverse direction. We review theoretical models relevant to resolution of this conflict. The winning role depends on a balance between the ‘value of winning’ and ‘power’ (relating to contest or armament costs): the winning role is likely to correlate with high value of winning and low costs. Sperm–ovum (or sperm–female tract) conflicts (and their plant parallels) are likely to obey the same principles. Males may typically have higher values of winning, but it is difficult to quantify ‘power’, and females may often be able to resist mating more cheaply than males can force it. We tentatively predict that sexual conflict will typically result in a higher rate of speciation in ‘female–win’ clades, that females will be responsible for premating isolation through reinforcement, and that ‘female–win’ populations will be less genetically diverse.

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A comparison of reproductive isolation between two closely related oak species in zones of recent and ancient secondary contact

BMC Evolutionary Biology ◽

10.1186/s12862-019-1399-y ◽

2019 ◽

Vol 19 (1) ◽

Cited By ~ 2

Author(s):

Wan-Jin Liao ◽

Bi-Ru Zhu ◽

Yue-Fei Li ◽

Xiao-Meng Li ◽

Yan-Fei Zeng ◽

...

Keyword(s):

Reproductive Isolation ◽

Secondary Contact

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Rapid polygenic response to secondary contact in a hybrid species

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2017.0365 ◽

2017 ◽

Vol 284 (1853) ◽

pp. 20170365 ◽

Cited By ~ 4

Author(s):

Glenn-Peter Sætre ◽

Angélica Cuevas ◽

Jo S. Hermansen ◽

Tore O. Elgvin ◽

Laura Piñeiro Fernández ◽

...

Keyword(s):

Interspecific Competition ◽

Neural Development ◽

Genetic Divergence ◽

Bird Species ◽

Secondary Contact ◽

Parent Species ◽

Significant Drop ◽

Genetic Changes ◽

Hybrid Species ◽

Feeding Site

Secondary contact between closely related species can have genetic consequences. Competition for essential resources may lead to divergence in heritable traits that reduces interspecific competition leading to increased rate of genetic divergence. Conversely, hybridization and backcrossing can lead to genetic convergence. Here, we study a population of a hybrid species, the Italian sparrow ( Passer italiae ), before and after it came into secondary contact with one of its parent species, the Spanish sparrow ( P. hispaniolensis ), in 2013. We demonstrate strong consequences of interspecific competition: Italian sparrows were kept away from a popular feeding site by its parent species, resulting in poorer body condition and a significant drop in population size. Although no significant morphological change could be detected, after only 3 years of sympatry, the Italian sparrows had diverged significantly from the Spanish sparrows across a set of 81 protein-coding genes. These temporal genetic changes are mirrored by genetic divergence observed in older sympatric Italian sparrow populations within the same area of contact. Compared with microallopatric birds, sympatric ones are genetically more diverged from Spanish sparrows. Six significant outlier genes in the temporal and spatial comparison (i.e. showing the greatest displacement) have all been found to be associated with learning and neural development in other bird species.

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THE LESSONIA NIGRESCENS SPECIES COMPLEX (LAMINARIALES, PHAEOPHYCEAE) SHOWS STRICT PARAPATRY AND COMPLETE REPRODUCTIVE ISOLATION IN A SECONDARY CONTACT ZONE1

Journal of Phycology ◽

10.1111/j.1529-8817.2011.01019.x ◽

2011 ◽

Vol 47 (4) ◽

pp. 894-903 ◽

Cited By ~ 41

Author(s):

Florence Tellier ◽

Javier Tapia ◽

Sylvain Faugeron ◽

Christophe Destombe ◽

Myriam Valero

Keyword(s):

Reproductive Isolation ◽

Species Complex ◽

Secondary Contact ◽

Lessonia Nigrescens

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Extensive introgression despite Haldane’s rule: insights from grasshopper hybrid zones

10.22541/au.163785413.32517525/v1 ◽

2021 ◽

Author(s):

Linda Hagberg ◽

Enrique Celemin ◽

Iker Irisarri ◽

Oliver Hawlitschek ◽

J L Bella ◽

...

Keyword(s):

Gene Flow ◽

Reproductive Isolation ◽

Male Sterility ◽

Secondary Contact ◽

Hybrid Zones ◽

Hybrid Male ◽

Hybrid Male Sterility ◽

Haldane’S Rule ◽

Haldane's Rule ◽

Species Formation

Although the process of species formation is notoriously idiosyncratic, the observation of pervasive patterns of reproductive isolation across species pairs suggests that generalities, or “rules”, underlie species formation in all animals. Haldane’s rule states that whenever a sex is absent, rare or sterile in a cross between two taxa, that sex is usually the heterogametic sex. Yet, understanding how Haldane’s rule first evolves and whether it is associated to genome wide barriers to gene flow remains a challenging task because this rule is usually studied in highly divergent taxa that no longer hybridize in nature. Here, we address these questions using the meadow grasshopper Pseudochorthippus parallelus where populations that readily hybridize in two natural hybrid zones show hybrid male sterility in laboratorial crosses. Using mitochondrial data, we infer that such populations have diverged some 100,000 years ago, surviving multiple glacial periods in isolated Pleistocenic refugia. Nuclear data shows that secondary contact has led to extensive introgression throughout the species range, including between populations showing hybrid male sterility. We find repeatable patterns of genomic differentiation across the two hybrid zones, yet such patterns are consistent with shared genomic constraints across taxa rather than their role in reproductive isolation. Together, our results suggest that Haldane’s rule can evolve relatively quickly within species, particularly when associated to strong demographic changes. At such early stages of species formation, hybrid male sterility still permits extensive gene flow, allowing future studies to identify genomic regions associated with reproductive barriers.

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Parental population range expansion before secondary contact promotes heterosis

10.1101/2020.04.28.066308 ◽

2020 ◽

Author(s):

Ailene MacPherson ◽

Silu Wang ◽

Ryo Yamaguchi ◽

Loren H. Riesesberg ◽

Sarah P. Otto

Keyword(s):

Reproductive Isolation ◽

Range Expansion ◽

Genomic Analysis ◽

Population Expansion ◽

Ancestral Population ◽

Secondary Contact ◽

Hybrid Zones ◽

Deleterious Alleles ◽

Genomic Divergence ◽

Slightly Deleterious Mutations

AbstractPopulation genomic analysis of hybrid zones is instrumental to our understanding of the evolution of reproductive isolation. Many temperate hybrid zones are formed by the secondary contact between two parental populations that had undergone post-glacial range expansion. Here we show that explicitly accounting for historical parental isolation followed by range expansion prior to secondary contact is fundamental for explaining genetic and fitness patterns in these hybrid zones. Specifically, ancestral population expansion can result in allele surfing, neutral or slightly deleterious mutations drift high frequency at the front of the expansion. If these surfed deleterious alleles are recessive, they can contribute to substantial heterosis in hybrids produced at secondary contact, counteracting negative-epistatic interactions between BDMI loci and hence can deteriorate reproductive isolation. Similarly, surfing at neutral loci can alter the expected pattern of population ancestry and suggests that accounting for historical population expansion is necessary to develop accurate null genomic models in secondary-contact hybrid zones. Furthermore, this process should be incorporated in macroevolutionary models of divergence as well, since such heterosis facilitated by parental-range expansion could dampen genomic divergence established in the past.

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Rapid and recent allopatric speciation in firs from central Mexico: evidence for reinforcement?

10.22541/au.162064326.66276060/v1 ◽

2021 ◽

Author(s):

Gustavo Giles-Pérez ◽

Erika Aguirre-Planter ◽

Luis Eguiarte ◽

Juan Jaramillo-Correa

Keyword(s):

Reproductive Isolation ◽

Volcanic Belt ◽

Secondary Contact ◽

Reproductive Phenology ◽

Central Mexico ◽

Sky Islands ◽

Hybrid Fitness ◽

Mexican Volcanic Belt ◽

History Of ◽

Self Fertilization

Secondary contact of species that have evolved partial reproductive isolation in allopatry may result in several outcomes, which range from rampant hybridization to barrier reinforcement. Reinforcement arises from reduced hybrid fitness, which promotes assortative mating and hence speciation. In plants, self-fertilization and disjunctions in reproductive-phenology are often invoked as evidence of reinforcement. However, local adaptation and pleiotropic effects during colonization can also lead to reproductive isolation without reinforcement. We explored these possibilities in a fir species complex (Abies flinckii - A. religiosa) distributed in ‘sky-islands’ along the Trans-Mexican Volcanic Belt (TMVB), in central Mexico. Despite co-occurring in two independent sympatric regions (west and center), these two taxa seem to rarely interbreed because of disjunct reproductive phenologies. We genotyped 1,147 SNPs, generated by GBS across 23 populations, and compared multiple demographic scenarios, built based on the geological history of the TMVB. The best-fitting model suggested a recent species split (for a conifer), dating back to ~1.2 Ma, together with early asymmetric gene flow (mostly from A. flinckii into A. religiosa), limited to the central sympatric region. Coupled with the lack of support for colonization models, the summary statistics (f, Hobs, FST, θπ, etc.) and historical demographic inferences made herein point to a rapid speciation with an early development of reinforcement, as a putative mechanism for avoiding hybridization. The role of reinforcement should be thus further explored in the (sub)tropics, as likely explanation for how species diversity is generated and maintained.

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Pre- and post-mating reproductive isolation evolve independently during rapid adaptation to high temperature

10.1101/2021.11.08.467720 ◽

2021 ◽

Author(s):

Sheng-Kai Hsu ◽

Wei-Yun Lai ◽

Johannes Novak ◽

Felix Lehner ◽

Ana Marija Jakšić ◽

...

Keyword(s):

Reproductive Isolation ◽

Natural Populations ◽

Cuticular Hydrocarbon ◽

Ecological Speciation ◽

Temperature Adaptation ◽

Rapid Adaptation ◽

Epistatic Interactions ◽

Males And Females ◽

Altered Lipid Metabolism ◽

Altered Lipid

Ambient temperature is one major ecological factor driving adaptation in natural populations, but its impact on the emergence of new species is not yet clear. Here, we explored the evolution of reproductive isolation during temperature adaptation by exposing 10 replicate Drosophila simulans populations to a hot temperature regime. Within less than 200 generations, both pre- and post-mating reproductive isolation evolved. The altered lipid metabolism of evolved flies also affected the cuticular hydrocarbon (CHCs) profiles. Different CHC profiles could explain the emerged assortative mating between ancestral and evolved populations. Hence, we identified the hallmark of ecological speciation driven by temperature adaptation. While this pre-mating isolation occurred only between ancestral and evolved replicate populations, post-mating reproductive isolation was observed among evolved replicate populations. We propose that epistatic interactions of reproduction-related genes between males and females resulted in adaptive co-evolution. Incompatibilities between different gene combinations favored in each replicate could explain the observed post-mating reproductive isolation. We anticipate that this mutation-order-like speciation from standing genetic variation, a new speciation process, is widespread in nature when highly polygenic traits are involved in adaptation.

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Geographic and Ecological Dimensions of Host Plant-Associated Genetic Differentiation and Speciation in the Rhagoletis cingulata (Diptera: Tephritidae) Sibling Species Group

Insects ◽

10.3390/insects10090275 ◽

2019 ◽

Vol 10 (9) ◽

pp. 275 ◽

Cited By ~ 6

Author(s):

Doellman ◽

Schuler ◽

Jean ◽

Hood ◽

Egan ◽

...

Keyword(s):

Reproductive Isolation ◽

Sibling Species ◽

Adaptive Radiation ◽

Ecological Theory ◽

Species Group ◽

Secondary Contact ◽

Similar Species ◽

Isolated Populations ◽

Ecological Diversification ◽

Postzygotic Reproductive Isolation

Ascertaining the causes of adaptive radiation is central to understanding how new species arise and come to vary with their resources. The ecological theory posits adaptive radiation via divergent natural selection associated with novel resource use; an alternative suggests character displacement following speciation in allopatry and then secondary contact of reproductively isolated but ecologically similar species. Discriminating between hypotheses, therefore, requires the establishment of a key role for ecological diversification in initiating speciation versus a secondary role in facilitating co-existence. Here, we characterize patterns of genetic variation and postzygotic reproductive isolation for tephritid fruit flies in the Rhagoletis cingulata sibling species group to assess the significance of ecology, geography, and non-adaptive processes for their divergence. Our results support the ecological theory: no evidence for intrinsic postzygotic reproductive isolation was found between two populations of allopatric species, while nuclear-encoded microsatellites implied strong ecologically based reproductive isolation among sympatric species infesting different host plants. Analysis of mitochondrial DNA suggested, however, that cytoplasmic-related reproductive isolation may also exist between two geographically isolated populations within R cingulata. Thus, ecology associated with sympatric host shifts and cytoplasmic effects possibly associated with an endosymbiont may be the key initial drivers of the radiation of the R. cingulata group.

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Vocal recognition suggests premating isolation between lineages of a lekking hummingbird

Behavioral Ecology ◽

10.1093/beheco/araa050 ◽

2020 ◽

Vol 31 (4) ◽

pp. 1046-1053 ◽

Cited By ~ 1

Author(s):

Nataly Cruz-Yepez ◽

Clementina González ◽

Juan Francisco Ornelas

Keyword(s):

Reproductive Isolation ◽

Distinct Species ◽

Secondary Contact ◽

Phenotypic Traits ◽

Premating Isolation ◽

Song Recognition ◽

Sierra Madre ◽

Rapid Divergence ◽

Latency Response ◽

Song Playback

Abstract Species with genetically differentiated allopatric populations commonly differ in phenotypic traits due to drift and/or selection, which can be important drivers of reproductive isolation. Wedge-tailed sabrewing (Campylopterus curvipennis) is a species complex composed of three genetically and acoustically differentiated allopatric lineages that correspond to currently recognized subspecies in Mexico: C. c. curvipennis (Sierra Madre Oriental), C. c. pampa (Yucatán Peninsula), and C. c. excellens (Los Tuxtlas). Although excellens is taxonomically recognized as a distinct species, there is genetic evidence that lineages excellens and curvipennis have diverged from each other later than pampa. In this study, we experimentally tested C. c. curvipennis song recognition as a major factor in premating reproductive isolation for lineage recognition. To this end, we conducted a song playback experiment to test whether territorial males of one C. c. curvipennis lek discriminate among potential competitors based on male songs from the three lineages. Males of curvipennis responded more aggressively to songs of their own lineage and excellens, than to songs of the most divergent lineage pampa, as evidenced by significant differences in a variety of intensity and latency response variables. This indicate that the pampa male song does not represent a competitive threat as curvipennis and excellens songs, in which divergence and song recognition represent premating reproductive isolation between these isolated lineages. However, the acoustic limits between curvipennis and excellens might be attenuated by gene flow in case of secondary contact between them, despite the strong and relatively rapid divergence of their sexually selected song traits.

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