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Understanding the source of non-native introduced populations is crucial for forecasting geographic invasion potential and understanding the ecological consequences of potential establishment. Here we use genomics to identify the source populations and invasion dynamics of two non-native introduced populations from the iconic avian lineage of ‘great speciators’ known as white-eyes (genus Zosterops). We established confidently for the first time that introduced Zosterops populations in Hawaii and southern California are completely unrelated and derived from independent introductions of the species Z. japonicus and Z. simplex, respectively. We used descriptive population genetic statistics to identify a reduction in genetic diversity and increase in private alleles in the southern California population supporting a recent, potentially ongoing, genetic bottleneck in this population. In contrast, the introduced population in Hawaii showed no such characteristics, likely due to a larger founding population size and repeated introductions in this intentionally introduced population. Ecological niche modeling indicated that there is little environmentally suitable habitat for Z. simplex across the continent of North America, suggesting limited invasion potential, assuming niche conservatism. Yet, portions of the introduced Z. simplex population have already surpassed areas projected as suitable, likely because the urbanized environment of southern California offers biotic resources and microhabitats not captured by our model. Because Z. simplex appears to have overcome both the ‘invasion paradox’ of low founding genetic diversity and relatively unfamiliar environmental conditions in southern California, we suggest that this population may continue expanding beyond our environmental niche model projections in other temperate, urban regions.

Secondary contact between closely related taxa represents a "moment of truth" for speciation—an opportunity to test the efficacy of reproductive isolation that evolved in allopatry and to identify the genetic, behavioral, and/or ecological barriers that separate species in sympatry. Sex chromosomes are known to rapidly accumulate differences between species, an effect that may be exacerbated for neo-sex chromosomes that are transitioning from autosomal to sex-specific inheritance. Here we report that, in the Solomon Islands, two closely related bird species in the honeyeater family—Myzomela cardinalis and Myzomela tristrami—carry neo-sex chromosomes and have come into recent secondary contact after ~1.1 my of geographic isolation. Hybrids of the two species were first observed in sympatry ~100 years ago. To determine the genetic consequences of hybridization, we use population genomic analyses of individuals sampled in allopatry and in sympatry to characterize gene flow in the contact zone. Using genome-wide estimates of diversity, differentiation, and divergence, we find that the degree and direction of introgression varies dramatically across the genome. For sympatric birds, autosomal introgression is bidirectional, with phenotypic hybrids and phenotypic parentals of both species showing admixed ancestry. In other regions of the genome, however, the story is different. While introgression on the Z/neo-Z-linked sequence is limited, introgression of W/neo-W regions and mitochondrial sequence (mtDNA) is highly asymmetric, moving only from the invading M. cardinalis to the resident M. tristrami. The recent hybridization between these species has thus enabled gene flow in some genomic regions but the interaction of admixture, asymmetric mate choice, and/or natural selection has led to the variation in the amount and direction of gene flow at sex-linked regions of the genome. Author summary: When an invasive species colonizes an island and interacts with a closely related resident species, we are provided with a rare opportunity to study the consequences of interbreeding and the factors that keep species distinct. Regions of the genome that evolve rapidly and/or influence mate choice may be especially likely to act as incidental barriers to gene flow. The red Myzomela cardinalis, birds in the honeyeater family, have invaded Makira in the Solomon Islands, coming into contact with the endemic, all black Myzomela tristrami. We used population genomic analyses of individuals in geographic isolation, and those in geographic contact, to understand the history of these two species and the consequences of their recent range overlap. We found that sex-specific regions of the genome (i.e., sex chromosomes) were either limited in their ability to move between species, or only moved in one direction, from the invading M. cardinalis to the resident M. tristrami. This work highlights how certain regions of the genome may be especially important in defining species boundaries and the generation and maintenance of biodiversity. [ABSTRACT FROM AUTHOR]

Body size is a key morphological attribute, often used to delimit species boundaries among closely related taxa. But body size can evolve in parallel, reaching similar final states despite independent evolutionary and geographic origins, leading to faulty assumptions of evolutionary history. Here, we document parallel evolution in body size in the widely distributed leaf-nosed bat genus Hipposideros , which has misled both taxonomic and evolutionary inference. We sequenced reduced representation genomic loci and measured external morphological characters from three closely related species from the Solomon Islands archipelago, delimited by body size. Species tree reconstruction confirms the paraphyly of two morphologically designated species. The nonsister relationship between large-bodied H. dinops lineages found on different islands indicates that large-bodied ecomorphs have evolved independently at least twice in the history of this radiation. A lack of evidence for gene flow between sympatric, closely related taxa suggests the rapid evolution of strong reproductive isolating barriers between morphologically distinct populations. Our results position Solomon Islands Hipposideros as a novel vertebrate system for studying the repeatability of parallel evolution under natural conditions. We conclude by offering testable hypotheses for how geography and ecology could be mediating the repeated evolution of large-bodied Hipposideros lineages in the Solomon Islands. [ABSTRACT FROM AUTHOR]

The paradox of the great speciators describes a contradictory biogeographic pattern exhibited by numerous avian lineages in Oceania. Specifically, these lineages display broad geographic distributions across the region, implying strong over-water dispersal capabilities; yet, they also display repeated genetic and phenotypic divergence-even between geographically proximate islands-implying poor inter-island dispersal capabilities. One group originally cited as evidence for this paradox is the dwarf kingfishers of the genus Ceyx . Here, using genomic sequencing and comprehensive geographic sampling of the monophyletic Ceyx radiation from northern Melanesia, we find repeated, deep genetic divergence and no evidence for gene flow between lineages found on geographically proximate islands, providing an exceptionally clear example of the paradox of the great speciators. A dated phylogenetic reconstruction suggests a significant burst of diversification occurred rapidly after reaching northern Melanesia, between 3.9 and 2.9 MYA. This pattern supports a shift in net diversification rate, concordant with the expectations of the "colonization cycle" hypothesis, which implies a historical shift in dispersiveness among great speciator lineages during the evolutionary past. Here, we present a formalized framework that explains how repeated founder effects and shifting selection pressures on highly dispersive genotypes are the only ultimate causes needed to generate the paradox of the great speciators. Within this framework, we emphasize that lineage-specific traits and island-specific abiotic factors will result in varying levels of selection pressure against dispersiveness, caused by varying proximate eco-evolutionary mechanisms. Overall, we highlight how understanding patterns of diversification in the Ceyx dwarf kingfishers helped us generate a cohesive framework that provides a rigorous mechanistic explanation for patterns concordant with the paradox of the great speciators and the repeated emergence of geographic radiations in island archipelagoes across the globe., (© The Author(s) 2024. Published by Oxford University Press on behalf of The Society for the Study of Evolution (SSE) and European Society for Evolutionary Biology (ESEN).)

Secondary contact between previously allopatric lineages offers a test of reproductive isolating mechanisms that may have accrued in isolation. Such instances of contact can produce stable hybrid zones-where reproductive isolation can further develop via reinforcement or phenotypic displacement-or result in the lineages merging. Ongoing secondary contact is most visible in continental systems, where steady input from parental taxa can occur readily. In oceanic island systems, however, secondary contact between closely related species of birds is relatively rare. When observed on sufficiently small islands, relative to population size, secondary contact likely represents a recent phenomenon. Here, we examine the dynamics of a group of birds whose apparent widespread hybridization influenced Ernst Mayr's foundational work on allopatric speciation: the whistlers of Fiji (Aves: Pachycephala ). We demonstrate two clear instances of secondary contact within the Fijian archipelago, one resulting in a hybrid zone on a larger island, and the other resulting in a wholly admixed population on a smaller, adjacent island. We leveraged low genome-wide divergence in the hybrid zone to pinpoint a single genomic region associated with observed phenotypic differences. We use genomic data to present a new hypothesis that emphasizes rapid plumage evolution and post-divergence gene flow.