Fig 1 PSMC plots: A) NW Europe (Red line) and S Europe (Blue line) sampled European nightjar, as well as pseudo-diploid genome of NW/S Europe birds (dashed line), depicting demographic history (Ne change) over the last ~5 million years (bp), scaled with a mutation rate of 4.6 × 10−9 per site and generation time of 2 years. The x-axis depicts time (in years) on a log scale, with the y-axis showing effective population size. B) Estimated Ne for pseudo-diploid genome only (dashed line). Approximate timings of significant periods of global climate change are shown by shading along the x-axis. Light blue shading = last glacial period (LGP), orange shading = Mid-Brunhes event (MBE), and dark blue shading = Mid-Pleistocene Revolution (MPR).
Overall, historic nightjar N e in Europe decreased and increased during periods of cooling and warming respectively (Fig 1a). Nightjar are insectivorous habitat specialists requiring clear fell, heathland, or woodland edge to breed (Cleere, 1998), feeding primarily on Lepidoptera (Mitchell et al., 2022). With reductions in temperature and glacial expansion, prey and habitat availability will have been constrained to more southerly latitudes (Schmitt, 2007), likely corresponding with a reduction in nightjar distribution and thus N e. For example, the decrease in nightjar N e ~1.2 Mya – ~ 600 Kya (Fig1a) overlapped the MPR (~1 Mya - 450 Kya), which was characterised by shortened interglacial periods and cooler average temperatures which restricted the northward resurgence of temperate animal and plant communities (Pisias and Moore, 1981; Head and Gibbard, 2015). Conversely, warmer temperatures will have likely increased the availability of suitable habitat across northerly latitudes (Schmitt, 2007; Candy et al., 2010). Indeed the stable climate of the late Pliocene and early Pleistocene (Head and Gibbard, 2015), as well as the short glacial and warm interglacial periods of the MBE (Candy et al., 2010; Barth et al., 2018) associated with increases in nightjarN e in our study (Fig 1a). Similarly, the dramaticN e increase during the late Pleistocene prior to the LGP (Fig 1a) coincided with the Eemian warm phase (~127 Kya; Bergoeing, 2017), which was characterised by the expansion and persistence of temperate plant communities into northerly latitudes (Van Andel and Tzedakis, 1996; Sánchez Goñi et al., 1999; Lisiecki and Raymo, 2005). Following similar trends exhibited by other Afro-Palearctic migrants (i.e Ficedcula flycatchers; Nadachowska-Brzyska et al., 2016), N e of both nightjar populations greatly decreased as the LGP continued, likely restricting nightjar to Southern European refugia (Schmitt, 2007; Lombardo et al., 2022) or North Africa (Thorup et al., 2021). Bootstrapping indicates caution is required regarding exact timings of N e fluctuations (Supporting Information). However, PSMC analysis in other Caprimulgids (i.e.: Chuck-will’s-widow) and Afro-Palearctic migrants (i.e.: Common cuckoo,Cuculus canorus ) (Nadachowska-Brzyska et al., 2015), have shown similar fluctuating trends inN e over the same timeframe, suggesting that the estimated timings of N e change with paleoclimatic events in our study are reasonable.
Population Structure and Divergence in Nightjar
When applied to a pseudo-diploid genome derived from two different populations, PSMC analysis can be used to determine the timing of population divergence. This is signalled by the pseudo-diploidN e diverging from the two parent populations and tending towards infinity (Prado-Martinez et al., 2013). This occurs because coalescence events between the two populations were severely reduced or ceased, leading to an increase inN e as interpreted by the analysis. In our analysis, the pseudo-diploid N e trend appeared to diverge from the NWE and SE populations ~1.2 Mya (Fig 1a). However, true divergence (the point at whichN e tends to infinity) does not occur until ~40 Kya (Fig 1b).Even taking into account f the ~35Ky error window suggested by the bootstrapping (Supporting Information), the main divergence event between the NWE and SE populations occurred within the LGP (Fig 1b).
The two modern populations used in this study are spatially distant and behaviorally distinct as they exhibit different migration strategies (Evens et al., 2017). Nightjars breeding in Western Europe typically migrate through Iberia during spring migration, with Eastern breeders migrating through Italy and SE Europe (Evens et al., 2017; Norevik et al., 2017). In other trans-Saharan migrants, such migratory behaviour is thought to be ancestral and ‘hard wired’ into populations, likely predating the Pleistocene (Thorup et al., 2021). Although the SE bird in our study was trapped during the spring migration period (Secomandi et al., 2021), it is probable that the individual’s breeding population was located within Central to Eastern Europe as suggested by recent tracking studies (e.g., Norevik et al., 2017).
As in other migratory Palearctic birds (e.g., Lesser whitethroatSylvia curruca ; Olsson et al., 2013; Pied wagtail Motacilla alba ; Li et al., 2016), we suggest that nightjar may exhibit East-West genetic structuring, but investigation is required. Results from MtDNA analysis have suggested that nightjar can be divided into Eastern and Western lineages, with divergence being deeper (c. 2.9 Mya) (Schweizer et al., 2020) than that suggested by our PSMC analysis (initial divergence ~1.2 Mya, cessation of gene flow ~40 Kya ± 35 Ky; Fig 1). However, the samples contributing to Schweizer et al.’s (2020) work spanned a much broader latitudinal range (encompassing W Europe to Asia) than those in our study and likely represented a deeper divergence. Much of the structure in contemporary Palearctic and Nearctic animal populations are fundamentally linked to past glacial and interglacial cycles, which have led to the contraction of temperate breeding populations into Southern refugia, and subsequent northward recolonisation during warmer interglacial periods (Hewitt, 2004; Nadachowska-Brzyska et al., 2016; Yao et al., 2022; de Greef et al., 2022). Previously panmictic populations may become isolated from one another in different refugia, during periods of glaciation, leading to genetic differentiation post-interglacial expansion (Hewitt et al., 2001).
Considering the timings of gene flow reduction and divergence between the two populations it is likely that the ancestral states of both populations utilised different refugia over historic glacial periods and most recently the LGM. Owing to the apparent divide in contemporary migration routes we suggest that the NWE population will have utilised the Iberia refugium and the SE sampled population the Italian refugia during glacial periods. Whilst most Western Palearctic avifauna (117 out of 131 studied by Pârâu and Wink, 2021) show admixture among populations, our study suggests that nightjar exhibit genetic structure within their Eurasian breeding range. With the sampling information available our results tentatively reflect East-West structuring in the European nightjar population, likely diverging during isolation in different glacial refugia during periods of glaciation. However, it should be noted that the SE individual may belong to the Southern European C.e.meridionalis subspecies and instead our results might reflect divergence between C.e.meridionalis and the nominate C.e.europaeus (NWE individual) subspecies. Nevertheless, validity of the C.e.meridionalis subspecies remains questionable, with as yet no genetic evidence to support the subspecies status (Del Hoyo et al., 2014; BirdLife International, 2022). Nightjars of the nominate raceC.e.europaeus migrate through Italy and SE Europe (Evens et al., 2017; Norevik et al., 2017). Given the individual used in this study was sampled during spring migration, it is likely that the bird was migrating to breeding grounds at a higher latitude and belongs toC.e.europaeus . However, further work is required to resolve population genetic structure across the species range, and there is a wider need to resolve the molecular phylogeny of European nightjar and its subspecies.
Evolution of Migratory Behaviour in Nightjar
Following the timeline proposed by our study (Fig 1), it seems unlikely that nightjar migratory behaviour developed post-LGM as suggested by Larsen et al., (2007). The dramatically fluctuating N e prior to the LGM throughout the Pleistocene may reflect periods of significant population expansion and contraction associated with climate driven changes in temperate breeding habitat availability (Ponti et al., 2020). If nightjar had exhibited a sedentary Afrotropic distribution prior to the LGM we might expect to see less severe fluctuation inN e relative to global climate change (Kimmitt et al., 2023; but see Speckled mousebird; Colius striatus in Nadachowska-Brzyska et al., 2015). Similarly, if migratory behaviour had not developed until ~20,000 ya, we would expect divergence between populations to occur exclusively post-LGM. However, our results highlight that whilst gene flow appeared to cease between the NWE and SE populations towards the LGM (Fig 1b), population divergence occurred as early as ~1.2 Mya (Fig 1a), with subsequent episodes of mixing ensued during periods of range expansion. Our results suggest that long-distance migratory behaviour in nightjar evolved prior to the LGM and was maintained throughout the Pleistocene, likely predating the initial divergence 1.2Mya recorded in our study (Fig 1a). This is corroborated by the deeper divergence (2.9Mya) between range-wide East-West lineages recorded by Schweizer et al., (2020), which may indicate a migratory divide. Our results contribute to the growing consensus that long distance migratory behaviour in contemporary Western-Palearctic avifauna predates the LGM (i.e. Ponti et al., 2020; Ralston et al., 2021; Thorup et al., 2021; Kimmitt et al., 2023).
Limitations of PSMC analysis
Results of PSMC analysis are influenced by the scaling applied to plots, determined by mutation rate and generation time (Li and Durbin, 2011; Mather et al., 2019). However), the overall pattern ofN e change will remain the same independent of scaling parameters (Nadachowska-Brzyska et al., 2016). Data on both of these parameters are often limited for study species (e.g. see Sato et al., 2020; Chattopadhyay et al., 2019; Ericson et al., 2022), including nightjar. Thanks to the wealth of PSMC studies over a multitude of avian taxa (e.g., Nadachowska-Brzyska et al., 2015, 2016; Kozma et al., 2018; Sato et al., 2020; Brüniche-Olsen et al., 2021) parameters suited to a wide range of avifauna can be selected, such as those used in our study as per Sato et al., (2020). Therefore, whilst caution must be applied concerning the timings and magnitudes of N e change, as highlighted by bootstrapping (see Supporting Information), we believe that PSMC analysis provides a valuable method to associate broadN e trends concurrent climate cycles.
Conclusion
PSMC is a useful tool to characterise past demography and resolve timing of species and population differentiation, processes which underlie contemporary genetic and demographic patterns. Results from our PSMC analysis suggest that nightjar were highly susceptible to climatic variation, increasing in number during warm interglacials and long periods of relative climate stability. The historical context provided by our research suggests that the current climate best suits nightjar. Limitations on population size are likely primarily anthropogenic, with humans responsible for the mass deforestation and agriculturalisation of Europe from 8.2 Kya (Kaplan et al. 2009). Habitat loss, fragmentation, degradation and disturbance are reported as the primary drivers of contemporary population reduction in nightjar (Langston et al., 2007; Lowe et al., 2014; Ashpole et al., 2015). Although nightjar have been shown to persist through historic climate change, contemporary anthropogenic pressures may reduce the ability of the species to adapt to the current rapidly changing climate.
As in multiple other Palearctic and Nearctic birds, our analysis suggests that restriction to different refugia during glacial cycles may have driven divergence within the European population of nightjar. Our analysis suggests a complete cessation of gene flow between the two populations by ~14 Kya during the LGM, although mixing under current interglacial conditions is likely. Genetic structure within the European population has significant conservation implications, potentially delimiting the current population into smaller conservation units. Our results also suggest that migratory behaviour in nightjar evolved prior to the LGM, persisting throughout the Pleistocene. However, further research is needed to understand the spatial context of this apparent range-wide genetic structure, as well as to clarify timing of long-distance migration evolution, as well as current taxonomic assignations. We recommend a range-wide molecular analysis, including population genetics, of nightjar to better understand the extent and origins of divergence within the species. Such research would also aid ongoing taxonomic uncertainties surrounding subspeciation in nightjar (Schweizer et al., 2020). Finally, while caution is needed, here PSMC analysis has provided a useful insight into the demographic past of nightjar in Europe, which has highlighted the nightjar population genetics as a valuable future research direction.
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