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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)
Stockholm University, Faculty of Science, Department of Zoology, Systematic Zoology. Swedish Museum of Natural History, Sweden; Museum für Naturkunde, Germany.ORCID iD: 0000-0002-8812-9313
Stockholm University, Faculty of Science, Department of Zoology, Systematic Zoology. Swedish Museum of Natural History, Sweden; Museum für Naturkunde, Germany.ORCID iD: 0000-0002-8173-7877
Stockholm University, Faculty of Science, Department of Zoology, Ethology.ORCID iD: 0000-0002-3807-4983
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Number of Authors: 92024 (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.

Place, publisher, year, edition, pages
2024. Vol. 19, no 5, article id e0293715
National Category
Evolutionary Biology Genetics and Genomics
Identifiers
URN: urn:nbn:se:su:diva-235793DOI: 10.1371/journal.pone.0293715ISI: 001231237700055PubMedID: 38781204Scopus ID: 2-s2.0-85194129569OAI: oai:DiVA.org:su-235793DiVA, id: diva2:1915299
Available from: 2024-11-22 Created: 2024-11-22 Last updated: 2025-04-25Bibliographically approved
In thesis
1. Speciation dynamics of New Guinean birds using large scale museomics
Open this publication in new window or tab >>Speciation dynamics of New Guinean birds using large scale museomics
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
speciation, museomics, birds, phylogeography, biogeography, population genetics, hybridisation
National Category
Evolutionary Biology
Research subject
Systematic Zoology
Identifiers
urn:nbn:se:su:diva-242517 (URN)978-91-8107-276-1 (ISBN)978-91-8107-277-8 (ISBN)
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, 2019-­03900
Available from: 2025-05-21 Created: 2025-04-25 Last updated: 2025-05-13Bibliographically approved

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Müller, Ingo A.Thörn, FilipRajan, Samyuktha

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