Late Miocene origin and recent population collapse of the Malagasy savanna olive tree (Noronhia lowryi)

Salmona, Jordi; Olofsson, Jill K.; Hong‐Wa, Cynthia; Razanatsoa, Jacqueline; Rakotonasolo, Franck; Ralimanana, Hélène; Randriamboavonjy, Tianjanahary; Suescun, Uxue; Vorontsova, Maria S.; Besnard, Guillaume

doi:10.1093/biolinnean/blaa036

Cited by 13 publications

(42 citation statements)

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“…The inferred decline and population subdivision of M. sp. #3 was initiated long before anthropogenic land use, supporting the emerging consensus that human colonization in Madagascar alone does not explain the occurrence of open habitats and isolated forest fragments (Quéméré et al 2012;Vorontsova et al 2016;Yoder et al 2016;Salmona et al 2017Salmona et al , 2020Hackel et al 2018 (Fig. 6B).…”

Section: Population Size Dynamicssupporting

confidence: 52%

Cryptic Patterns of Speciation in Cryptic Primates: Microendemic Mouse Lemurs and the Multispecies Coalescent

et al. 2020

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Abstract Mouse lemurs (Microcebus) are a radiation of morphologically cryptic primates distributed throughout Madagascar for which the number of recognized species has exploded in the past two decades. This taxonomic revision has prompted understandable concern that there has been substantial oversplitting in the mouse lemur clade. Here, we investigate mouse lemur diversity in a region in northeastern Madagascar with high levels of microendemism and predicted habitat loss. We analyzed RADseq data with multispecies coalescent (MSC) species delimitation methods for two pairs of sister lineages that include three named species and an undescribed lineage previously identified to have divergent mtDNA. Marked differences in effective population sizes, levels of gene flow, patterns of isolation-by-distance, and species delimitation results were found among the two pairs of lineages. Whereas all tests support the recognition of the presently undescribed lineage as a separate species, the species-level distinction of two previously described species, M. mittermeieri and M. lehilahytsara is not supported – a result that is particularly striking when using the genealogical discordance index (gdi). Non-sister lineages occur sympatrically in two of the localities sampled for this study, despite an estimated divergence time of less than 1 Ma. This suggests rapid evolution of reproductive isolation in the focal lineages, and in the mouse lemur clade generally. The divergence time estimates reported here are based on the MSC calibrated with pedigree-based mutation rates and are considerably more recent than previously published fossil-calibrated relaxed-clock estimates. We discuss the possible explanations for this discrepancy, noting that there are theoretical justifications for preferring the MSC estimates in this case.

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Section: Population Size Dynamicssupporting

confidence: 52%

Cryptic Patterns of Speciation in Cryptic Primates: Microendemic Mouse Lemurs and the Multispecies Coalescent

et al. 2020

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“…First, a better fit of all recent forest cover [2000’s; (Hansen et al ., 2013; Vieilledent et al ., 2018)], compared to older vegetation cover (1953, 1973), suggests that the small forest changes that have occurred through this period (Quéméré et al ., 2012) are unable to explain the genetic diversity of N. spinifolia. Second, because we sampled and genotyped mostly fully-grown and mature trees, and since the generation time of Noronhia is potentially long [>20-50 years; (Salmona et al ., 2020)], its estimated genetic diversity is expected to reflect ancient (e.g. ~50-100 years old) forest cover.…”

Section: Discussionmentioning

confidence: 99%

“…Although deforestation has greatly intensified across Madagascar (~40-50%) since the 1950’s (Harper et al ., 2007; Vieilledent et al ., 2018), it has also remained surprisingly mild in some regions like the Loky-Manambato (northern-Madagascar) (Quéméré et al ., 2012). Furthermore, the Miocene expansion of the Malagasy savannas (Vorontsova et al ., 2016; Hackel et al ., 2018; Solofondranohatra et al ., 2018; Salmona et al ., 2020) evidenced the antiquity of open-canopy environments. In some regions, it therefore remains crucial to confirm the questionable antiquity of landscapes and to identify their related change-inducing factors [e.g.…”

Section: Introductionmentioning

confidence: 99%

“…We first tested whether its restricted geographic distribution resulted in a low genetic diversity, as expected under a neutral model (Kimura, 1983), or remained relatively high as for co-distributed primates [ P. tattersalli and Microcebus tavaratra (Quéméré et al ., 2010; Aleixo-Pais et al ., 2019)]. We then inferred the effect of landscape components on maternally and biparentally inherited genetic diversity, to investigate patterns of seed and pollen dispersals, and assessed their congruence with those of a congeneric species from the High Plateau [ N. lowryi (Salmona et al , 2020)], and of co-distributed taxa (abovementioned). We also examined whether the relative stability of the forest cover in the past 70 years (Quéméré et al ., 2012; Salmona et al ., 2017b) is reflected in N. spinifolia genetic makeup, comparing the effect of recent and historical forest covers on gene flow, as a proxy for the temporality of its habitat fragmentation.…”

Section: Introductionmentioning

confidence: 99%

“…Deforestation is among the greatest drivers of biodiversity and habitat loss, and fragmentation in Madagascar [~40-50% area since the 1950’s (Harper et al ., 2007; Vieilledent et al ., 2018)]. However, the recent documentation of the Miocene origin of the Malagasy grassland endemics (Bond et al ., 2008; Vorontsova et al ., 2016; Hackel et al ., 2018; Solofondranohatra et al ., 2018; Salmona et al ., 2020) sparked a hot debate on the antiquity of open-canopy environments (Godfrey & Crowley, 2016; Joseph & Seymour, 2020, 2021). Since the genetic diversity of an organism, and its conservation implications, are the combined results of its distribution structure and history, it is crucial to assess the antiquity of landscapes, which can be questioned from genetic data [e.g.…”

Section: Introductionmentioning

confidence: 99%

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How ancient forest fragmentation and riparian connectivity generate high levels of genetic diversity in a microendemic Malagasy tree

Salmona

Dresen

Ranaivoson

et al. 2020

Preprint

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Understanding landscape changes is central to predicting evolutionary trajectories and defining conservation practices. While human-driven deforestation is intense throughout Madagascar, exception in areas like the Loky-Manambato region (North) raises questions. This region also harbors a rich and endemic flora, whose evolutionary origin remains poorly understood.We assessed the genetic diversity of an endangered micro-endemic Malagasy olive species (Noronhia spinifolia) to better understand the vegetation dynamic in the Loky-Manambato region and its influence on past evolutionary processes. We characterized 72 individuals sampled across eight forests through nuclear and mitochondrial restriction associated sequencing data (RADseq) and chloroplast microsatellites (cpSSR).Extremely high genetic diversity was revealed in the three genomic compartments (chloroplast h = 0.99, mitochondrial h = 0.85, and nuclear HO = 0.07-0.20). Combined population and landscape genetics analyses indicate that N. spinifolia diversity is best explained by the current forest cover (R2 = 0.90), highlighting a long-standing forest fragmentation in the region. Our results further suggest a predominant role of forestdwelling organisms in mediating pollen and seed dispersals.This sustains a major and long-term role of riparian corridors in maintaining connectivity across those antique mosaic-habitats, calling for the study of organismal interactions that promote gene flow.

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The grassy ecosystems of Madagascar in context: Ecology, evolution, and conservation

Silander,

Bond,

Ratsirarson

2023

Plants People Planet

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Societal Impact StatementMadagascar is famous for its unique forests and their fauna. Most of the island is covered by flammable grassy ecosystems long considered to be of human origin and threatening the remaining forests. Yet new studies show that many plants and animals of the grassy systems are unique to Madagascar and restricted to these open habitats. Open grassy ecosystems have markedly different management requirements from forests and bring different contributions to society. We argue that the grassy ecosystems can benefit Madagascar if understood and managed wisely using expanded knowledge bases that also include collaboration with locals.SummaryUntil recently, nearly all research and interests in Madagascar focused on forested habitats. To help place Madagascar's grassy ecosystems in context, we provide a summary of the origin, development, and evolution of open tropical, C4 grassy ecosystems elsewhere, especially those from Africa; we summarize similarities and differences with the distribution of C3 and C4 grasses in the Malagasy landscape, their plant traits, and inferences on the evolutionary legacy of grasses. We also discuss the animal communities that use and have coevolved in these grassy systems; to help resolve controversies over the pre‐settlement extent of grassy ecosystems, we suggest a variety of complementary geochemical, palaeobotanical, and molecular genetic tools that have been effectively used elsewhere to untangle forest/grassy ecosystem mosaics and the ecological and evolutionary processes that influence them. Many of these tools can and should be employed in Madagascar to fully understand the spatio‐temporal dynamics of open, grassy, and closed forest systems across the island; as regards conservation, we discuss the ecosystem services provided by grassy systems, which are too often ignored in general, not only as a biome, vis‐à‐vis forests, but also for their global importance as a carbon sink and role they play in water management and providing goods to local villagers. We conclude by outlining the necessary research to better manage open ecosystems across Madagascar without threatening endangered forest ecosystems.

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Late Miocene origin and recent population collapse of the Malagasy savanna olive tree (Noronhia lowryi)

Cited by 13 publications

References 0 publications

Cryptic Patterns of Speciation in Cryptic Primates: Microendemic Mouse Lemurs and the Multispecies Coalescent

Cryptic Patterns of Speciation in Cryptic Primates: Microendemic Mouse Lemurs and the Multispecies Coalescent

How ancient forest fragmentation and riparian connectivity generate high levels of genetic diversity in a microendemic Malagasy tree

The grassy ecosystems of Madagascar in context: Ecology, evolution, and conservation

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