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Speciation dynamics of New Guinean birds using large scale museomics
Stockholm University, Faculty of Science, Department of Zoology. Department of Bioinformatics and Genetics, Swedish Museum of Natural History, Stockholm, Sweden; Museum für Naturkunde, Leibniz Institut für Evolutions- und Biodiversitätsforschung, Berlin, Germany.ORCID iD: 0000-0002-8812-9313
2025 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The overarching theme of this thesis was to investigate speciation histories and biogeographical patterns of New Guinean birds, by using whole genomes primarily extracted from natural history collections.

In Chapter I, I detected hidden diversity within the Lesser Melampitta, a species, which is widely distributed across different mountain ranges throughout New Guinea. In contrast, I found no strong differentiation between populations in the Greater Melampitta, a species characterised by a much more scattered distribution. I hypothesized that this unexpected pattern in the latter species may have been the result of a relatively recent collapse into its current fragmented distribution. Moreover, this chapter was instrumental in establishing and optimising bioinformatic workflows that I applied in the subsequent chapters. In Chapter II we investigated hybridisation patterns within a lineage of whistlers (Pachycephala). The study revealed a complex network of interactions between species that appears to be linked to geography. Species inhabiting islands and landmasses that were connected in the past during periods of lower sea levels were less differentiated and showed higher signals of introgression than species inhabiting more remote oceanic islands. Chapter III focussed on speciation dynamics within a genus of honeyeaters (Melidectes). The results support that most species within the genus have formed as a consequence of geographic isolation. However, two taxa with partially overlapping distributions in the central mountains of New Guinea, which are known to hybridise, exhibit a very complex genetic structure that does not follow the current species classification, as the hybridising taxa appear to be genetically indistinguishable. Yet, I recovered some genetic signals of past differentiation and consequently present this complex as a rare empirical example of ephemeral speciation. In addition, I investigated how future climate change may potentially result in new speciation events.  For Chapter IV, I investigated the extent of reproductive isolation and hybridisation patterns in the Birds-of-paradise genus Paradisaea and discuss the placement of various species along the speciation continuum. Unlike species with more isolated distributions, such as those found on islands surrounding New Guinea, three species on New Guinea’s mainland exhibit low genetic differentiation and a pattern of more or less unrestricted gene flow across much of the lowlands. An exception to this are the Lesser and Raggiana Birds-of-paradise that show marked genetic differentiation and the absence of ongoing gene flow. The population structure and differentiation of Paradisaea species on the New Guinean mainland thus closely resembles that of a ring species.

In the broader context, this thesis has demonstrated the value that historical DNA offers when studying speciation dynamics, especially for species and populations that are difficult to sample. Furthermore, it also highlights the impact of system-specific mechanisms which calls for caution when generalising conclusions within the field of speciation.

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University , 2025. , p. 36
Keywords [en]
speciation, museomics, birds, phylogeography, biogeography, population genetics, hybridisation
National Category
Evolutionary Biology
Research subject
Systematic Zoology
Identifiers
URN: urn:nbn:se:su:diva-242517ISBN: 978-91-8107-276-1 (print)ISBN: 978-91-8107-277-8 (electronic)OAI: oai:DiVA.org:su-242517DiVA, id: diva2:1954588
Public defence
2025-06-13, Lilla Hörsalen, Naturhistoriska riksmuseet, Frescativägen 40, and online via Zoom: Meeting ID: 662 1784 1202, Passcode: 373962, Stockholm, 13:00 (English)
Opponent
Supervisors
Funder
Swedish Research Council, 2019-­03900Available from: 2025-05-21 Created: 2025-04-25 Last updated: 2025-05-13Bibliographically approved
List of papers
1. Species-specific dynamics may cause deviations from general biogeographical predictions – evidence from a population genomics study of a New Guinean endemic passerine bird family (Melampittidae)
Open this publication in new window or tab >>Species-specific dynamics may cause deviations from general biogeographical predictions – evidence from a population genomics study of a New Guinean endemic passerine bird family (Melampittidae)
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2024 (English)In: PLOS ONE, E-ISSN 1932-6203, Vol. 19, no 5, article id e0293715Article in journal (Refereed) Published
Abstract [en]

The family Melampittidae is endemic to New Guinea and consists of two monotypic genera: Melampitta lugubris (Lesser Melampitta) and Megalampitta gigantea (Greater Melampitta). Both Melampitta species have scattered and disconnected distributions across New Guinea in the central mountain range and in some of the outlying ranges. While M. lugubris is common and found in most montane regions of the island, M. gigantaea is elusive and known from only six localities in isolated pockets on New Guinea with very specific habitats of limestone and sinkholes. In this project, we apply museomics to determine the population structure and demographic history of these two species. We re-sequenced the genomes of all seven known M. gigantaea samples housed in museum collections as well as 24 M. lugubris samples from across its distribution. By comparing population structure between the two species, we investigate to what extent habitat dependence, such as in M. gigantaea, may affect population connectivity. Phylogenetic and population genomic analyses, as well as acoustic variation revealed that M. gigantaea consists of a single population in contrast to M. lugubris that shows much stronger population structure across the island. We suggest a recent collapse of M. gigantaea into its fragmented habitats as an explanation to its unexpected low diversity and lack of population structure. The deep genetic divergences between the M. lugubris populations on the Vogelkop region, in the western central range and the eastern central range, respectively, suggests that these three populations should be elevated to full species level. This work sheds new light on the mechanisms that have shaped the intriguing distribution of the two species within this family and is a prime example of the importance of museum collections for genomic studies of poorly known and rare species.

National Category
Evolutionary Biology Genetics and Genomics
Identifiers
urn:nbn:se:su:diva-235793 (URN)10.1371/journal.pone.0293715 (DOI)001231237700055 ()38781204 (PubMedID)2-s2.0-85194129569 (Scopus ID)
Available from: 2024-11-22 Created: 2024-11-22 Last updated: 2025-04-25Bibliographically approved
2. Reticulate and hybrid speciation is promoted by environmental instability in an Indo-Pacific species complex of whistlers (Aves: Pachycephala)
Open this publication in new window or tab >>Reticulate and hybrid speciation is promoted by environmental instability in an Indo-Pacific species complex of whistlers (Aves: Pachycephala)
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(English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294XArticle in journal (Refereed) Submitted
Abstract [en]

Genomic studies have revealed introgressive hybridization as a common phenomenon across the tree of life, particularly among young radiations. As incipient speciation tends to be induced by vicariance events, it is assumed that introgressive hybridization is more frequent in young radiations in which allopatrically distributed species have a high probability of coming into secondary contact. In this study we utilize whole genomic data to investigate spatio-temporal introgression patterns in a songbird radiation that has colonized a highly dynamic island region in the Indo-Pacific. Some taxa within this radiation have colonized remote oceanic islands whereas others occur on landmasses and islands in the Sahul region that were periodically connected during Pleistocene periods of lower sea levels. Our results show that introgressive hybridization has been pervasive within this young radiation, despite prominent plumage differences between taxa. Geographical proximity has been an important factor for hybridization and we further find that species occupying islands in the environmentally unstable Sahul region exhibit particularly high signatures of introgressive hybridization. Yet, one species appears to have been shielded against hybridization, perhaps due to specific ecological specializations. Finally, we identify a hybrid species on an island where two oceanic radiations meet. Our results also caution against relying solely on analyses that only detect asymmetric introgression when examining systems with complex introgression histories. Collectively, our results support a growing body of literature that suggests that reticulate speciation is much more common than previously thought. This has implications for our understanding of species formation and their persistence through time.

Keywords
Hybridization, Birds, Population Dynamics, Speciation, Population Genetics, Genomics
National Category
Evolutionary Biology
Research subject
evolutionär genetik
Identifiers
urn:nbn:se:su:diva-242469 (URN)
Funder
Swedish Research Council, 2019-03900Knut and Alice Wallenberg Foundation, KAW 2020.0239
Available from: 2025-04-23 Created: 2025-04-23 Last updated: 2025-04-29
3. Ephemeral Speciation in a New Guinean Honeyeater Complex (Aves: Melidectes)
Open this publication in new window or tab >>Ephemeral Speciation in a New Guinean Honeyeater Complex (Aves: Melidectes)
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2025 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294XArticle in journal (Refereed) Epub ahead of print
Abstract [en]

Speciation is a fundamental concept in evolutionary biology, and understanding the mechanisms driving speciation remains the foremost research topic within this field. Hybridisation is often involved in speciation and can influence its rates, potentially accelerating, decelerating or even reversing the process. This study investigates the evolutionary history of the New Guinean bird genus Melidectes, consisting of six species that inhabit various montane regions at different elevations. While most Melidectes species have allopatric distributions, two species overlap in the central mountain range and hybridise. However, plumage differences and elevational adaptations are assumed to maintain the species' boundaries. Utilising specimens from natural history collections and comprehensive genomic analyses, including a de novo genome assembly, we characterise allopatric speciation patterns within the genus and highlight how future speciation could potentially be driven by climate change. Contrary to previous hypotheses, our findings suggest that in the two distributionally overlapping species, phenotypic differences do not prevent gene flow. We find limited acoustic differentiation and extensive admixture across most of their distributions. Divergence and admixture levels conform poorly to the current taxonomy and follow a geographical pattern in which the most isolated populations at the ends of the distributions are most divergent and show least admixture. However, in contrast, their mitochondrial genomes do group in accordance with species identity, namely, into two deeply divergent lineages. We propose that this system demonstrates the ephemeral nature of speciation, in which two incipient species have started mixing extensively as they came into secondary contact, resulting in nearly complete fusion into a single lineage.

Keywords
speciation, hybridisation, birds, molecular evolution, phylogeography, population genetics—empirical
National Category
Evolutionary Biology
Research subject
evolutionär genetik
Identifiers
urn:nbn:se:su:diva-242463 (URN)10.1111/mec.17760 (DOI)001464615800001 ()2-s2.0-105002435033 (Scopus ID)
Funder
Swedish Research Council, 2019‐03900Swedish Research Council, 2022‐06195
Available from: 2025-04-23 Created: 2025-04-23 Last updated: 2025-04-29
4. Speciation around a mountain chain: Hybridisation dynamics in a lek-mating Birds-of-paradise species complex (Paradisaea)
Open this publication in new window or tab >>Speciation around a mountain chain: Hybridisation dynamics in a lek-mating Birds-of-paradise species complex (Paradisaea)
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Speciation is a continuous process and understanding how incipient lineages evolve along this continuum remains a major challenge. Hybridisation and sexual selection play key roles in driving or constraining speciation, but their interaction can be complex. While strong mate choice should limit gene flow, interspecific hybridisation can lead to both lineage fusion or the introduction of genetic variants that can facilitate diversification. Birds-of-paradise provide a compelling system to explore these dynamics, as they exhibit some of the most elaborate forms of mate choice and sexually selected traits, and yet commonly hybridise. Using whole-genome sequencing of 108 historical specimens, we investigated phylogenetic relationships, gene flow, and genetic differentiation across the genus Paradisaea and its sister genus Paradisornis. Our results reveal species that vary in their relative position along the speciation continuum. While some allopatric species exhibit strong genetic differentiation, other species admix extensively even though they differ in plumage traits. The widespread mainland species complex (P. minor, P. apoda, and P. raggiana) in particular, follows a geographic gradient of genetic exchange, forming a pattern where geographically close populations show increasing admixture. Notwithstanding phenotypic variation in putatively sexually selected traits, the gradual shift in shared ancestry raises questions about the degree to which these taxa represent distinct species versus populations along a broader continuum of differentiation. Most strikingly, despite consistent signatures of genomic admixture between contiguous populations, P. minor and P. raggiana seem to be largely reproductively isolated in eastern New Guinea where the two lineages meet at the end of the central mountain range. The spatial distribution of divergence and hybridisation between P. minor, P. apoda, and P. raggiana, is therefore ring-like along the New Guinea highlands and presents a prime example of incipient lineages at different stages along the speciation continuum. Our findings illustrate how speciation can be simultaneously shaped by a complex interplay of geography, gene flow, and sexual selection, and how such processes in concert can lead to different stages of reproductive isolation across lineages and regions.

Keywords
speciation, phylogeography, hybridisation, birds, population genetics, molecular evolution
National Category
Evolutionary Biology
Research subject
evolutionär genetik
Identifiers
urn:nbn:se:su:diva-242515 (URN)
Funder
Swedish Research Council, 2019-­03900
Available from: 2025-04-25 Created: 2025-04-25 Last updated: 2025-04-25

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