Difference in plasticity of resting metabolic rate – the proximate explanation to different niche breadth in sympatricFicedulaflycatchers

Abstract

Variation in relative fitness of competing recently formed species across heterogeneous environments promotes coexistence. However, the physiological traits mediating such variation in relative fitness have rarely been identified. Resting metabolic rate (RMR) is tightly associated with life history strategies, thermoregulation, diet use, and inhabited latitude and could therefore moderate differences in fitness responses to fluctuations in local environments, particularly when species have adapted to different climates in allopatry. We work in a long‐term study of collared (Ficedula albicollis) and pied flycatchers (Ficedula hypoleuca) in a recent hybrid zone located on the Swedish island of Öland in the Baltic Sea. Here, we explore whether differences in RMR match changes in relative performance of growing flycatcher nestlings across environmental conditions using an experimental approach. The fitness of pied flycatchers has previously been shown to be less sensitive to the mismatch between the peak in food abundance and nestling growth among late breeders. Here, we find that pied flycatcher nestlings have lower RMR in response to higher ambient temperatures (associated with low food availability). We also find that experimentally relaxed nestling competition is associated with an increased RMR in this species. In contrast, collared flycatcher nestlings did not vary their RMR in response to these environmental factors. Our results suggest that a more flexible nestling RMR in pied flycatchers is responsible for the better adaptation of pied flycatchers to the typical seasonal changes in food availability experienced in this hybrid zone. Generally, subtle physiological differences that have evolved when species were in allopatry may play an important role to patterns of competition, coexistence, or displacements between closely related species in secondary contact.

Divergent mitochondrial and nuclear OXPHOS genes are candidates for genetic incompatibilities inFicedulaFlycatchers

“…This is not surprising given the larger starting population as well as the fact that the pied flycatcher population on Öland is not isolated to the same extent as the collared flycatcher population and hints at selection rather than demography leading to these patterns. This relatively higher diversity is consistent with the observed adaptive plasticity in pied flycatcher RMR and could be the result of a better adaption to the variable northern climate (McFarlane et al 2018). We interpret the marked divergence in OXPHOS-related genes (including fixation of different non-synonymous mutations in mtDNA) together with signs of positive selection in both mitochondrial and nuclear genes encoding OXPHOS proteins for complex I and III as a legacy of different climate adaptation from the recent time in allopatry (Qvarnström et al 2016).…”

“…Collared and pied flycatchers diverged less than 1 million years ago (Nadachowska-Brzyska et al 2013) with strong postzygotic reproductive isolation in the form of hybrid dysfunction and infertility (Ålund et al 2013, McFarlane et al 2016, Svedin et al 2008). Here, we specifically focus on divergence in mtDNA and the interacting nuclear OXPHOS genes, as we have recently demonstrated that phenotypic differences in metabolic rate play important roles related to both differences in niche breath of the two species (McFarlane et al 2018) and hybrid dysfunction (McFarlane et al 2016). Using data from free-living collared, pied and hybrid flycatchers, we demonstrate distinct divergence in both the mtDNA (Figure 2) and in OXPHOS-related nDNA (Figure 3) of these species.…”

“…Collared flycatchers displace pied flycatchers from the preferred breeding sites (Vallin et al 2012), but appear to be constrained to a narrower niche use, whereas pied flycatchers are less affected by a mismatch between food abundance and nestling growth (Qvarnström et al 2009, Sirkiä et al 2018). This robustness might be explained by higher plasticity in metabolic rate of pied flycatchers, as pied flycatcher nestlings have a lower resting metabolic rate (RMR) at higher temperatures (associated with low food availability) and increased RMR in response to relaxed sibling competition when compared to collared flycatchers (McFarlane et al 2018). The flexible RMR response to environmental conditions observed in pied flycatchers may allow pied flycatchers to breed in low quality habitat and late in the season when food availability is lower (McFarlane et al 2018).…”

“…This robustness might be explained by higher plasticity in metabolic rate of pied flycatchers, as pied flycatcher nestlings have a lower resting metabolic rate (RMR) at higher temperatures (associated with low food availability) and increased RMR in response to relaxed sibling competition when compared to collared flycatchers (McFarlane et al 2018). The flexible RMR response to environmental conditions observed in pied flycatchers may allow pied flycatchers to breed in low quality habitat and late in the season when food availability is lower (McFarlane et al 2018).…”

Differences in incubation behaviour and niche separation of two competing flycatcher species

“…Further, young pied flycatchers are often displaced from the preferred deciduous forests to mixed- and coniferous forest territories by collared flycatchers (Lundberg and Alatalo 1992 ; Qvarnstörm et al 2009 ; Veen et al 2010 ; Vallin et al 2012a , b ). Pied flycatcher nestlings also are better able to adjust their metabolism according to environmental changes (McFarlane et al 2018 ), which may partially explain their higher tolerance to low food availability. As incubation behaviour and thus the thermal environment during embryo development influences several physiological and developmental features of the off-spring, both in the short and longer term, it may thus also partly influence specie’s competitive ability and capacity to adapt to environmental changes.…”