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Cretaceous environmental changes led to high extinction rates in a hyperdiverse beetle family.

Kergoat GJ, Bouchard P, Clamens AL, Abbate JL, Jourdan H, Jabbour-Zahab R, Genson G, Soldati L, Condamine FL - BMC Evol. Biol. (2014)

Bottom Line: As attested by the fossil record, Cretaceous environmental changes have significantly impacted the diversification dynamics of several groups of organisms.Contrary to other insect groups, we found no support for a positive shift in diversification rates during the Cretaceous; instead there is evidence for an 8.5-fold increase in extinction rates that was not compensated by a joint increase in speciation rates.We hypothesize that this pattern is better explained by the concomitant reduction of arid environments starting in the mid-Cretaceous, which likely negatively impacted the diversification of arid-adapted species that were predominant at that time.

View Article: PubMed Central - PubMed

Affiliation: INRA - UMR 1062 CBGP (INRA, IRD, CIRAD, Montpellier SupAgro), Campus de Baillarguet, Montferrier-sur-Lez, 34988, France. kergoat@supagro.inra.fr.

ABSTRACT

Background: As attested by the fossil record, Cretaceous environmental changes have significantly impacted the diversification dynamics of several groups of organisms. A major biome turnover that occurred during this period was the rise of angiosperms starting ca. 125 million years ago. Though there is evidence that the latter promoted the diversification of phytophagous insects, the response of other insect groups to Cretaceous environmental changes is still largely unknown. To gain novel insights on this issue, we assess the diversification dynamics of a hyperdiverse family of detritivorous beetles (Tenebrionidae) using molecular dating and diversification analyses.

Results: Age estimates reveal an origin after the Triassic-Jurassic mass extinction (older than previously thought), followed by the diversification of major lineages during Pangaean and Gondwanan breakups. Dating analyses indicate that arid-adapted species diversified early, while most of the lineages that are adapted to more humid conditions diversified much later. Contrary to other insect groups, we found no support for a positive shift in diversification rates during the Cretaceous; instead there is evidence for an 8.5-fold increase in extinction rates that was not compensated by a joint increase in speciation rates.

Conclusions: We hypothesize that this pattern is better explained by the concomitant reduction of arid environments starting in the mid-Cretaceous, which likely negatively impacted the diversification of arid-adapted species that were predominant at that time.

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Related in: MedlinePlus

Maximum likelihood character trait optimization of habitat preferences. Ancestral character states that are significantly supported are highlighted using either an orange label (for “arid/semi-arid” habitat preferences) or a green label (for “other” habitat preferences). Grey labels indicate ancestral characters for which the difference in log-likelihood is lower than 2.0. For each genus, information on systematics is provided using abbreviated subfamilial and tribal names. A picture of a typical xerophilic species (Onymacris rugatipennis) is also included.
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Fig2: Maximum likelihood character trait optimization of habitat preferences. Ancestral character states that are significantly supported are highlighted using either an orange label (for “arid/semi-arid” habitat preferences) or a green label (for “other” habitat preferences). Grey labels indicate ancestral characters for which the difference in log-likelihood is lower than 2.0. For each genus, information on systematics is provided using abbreviated subfamilial and tribal names. A picture of a typical xerophilic species (Onymacris rugatipennis) is also included.

Mentions: Contrary to the arid-dwelling Pimeliinae, the other subfamilies are currently more diverse in tropical environments (see Matthews et al. [25] for details). Thus if we consider that phylogenetic biome conservatism holds in many groups [32], this suggests that distinct tenebrionid lineages were already adapted to arid or tropical environments before the end of the KTR. Results from character optimization analyses support this hypothesis and suggest that the common ancestor of tenebrionid beetles was adapted to arid environments (Figure 2). Arid environments were extremely widespread in the Early Jurassic [33,34]; though they progressively receded with the break-up of the Pangaea [6,7], they never completely disappeared, which could explain the persistence of distinct lineages of pimeliine beetles across eastern and western hemispheres [25]. Interestingly, pimeliine beetles are currently nearly absent from Australia, where aridification began in the Miocene and deserts only appeared very recently [35,36]. As underlined by Matthews et al. [25], this suggests that the group was strictly adapted to arid environments from the beginning, and unable to colonize the Australian continent before its isolation in the middle of the Cenozoic. The only exceptions are the few representatives (nine species) of two plesiotypic tribes (Cnemeplatiini and Vacronini) that were possibly present as coastal sand dune inhabitants before separation from Gondwana [37]. Other groups such as the rain-forest specialists Adeliini [29] originated about 96 Ma (median age of 95.13 Ma, 95% HPD: 82.69-113.95 Ma), possibly in the warm temperate forests that were widespread in the southern hemisphere at that time [4]. This is also the case for other tropical groups in the subfamily Tenebrioninae (tribes Heleini and Titaeini), whose most recent common ancestor diversified at the beginning of the Late Cretaceous, around 100 Ma (median age of 99.83 Ma, 95% HPD: 91.76-111.76 Ma). In some of these groups the phylogenetic biome conservatism is not irreversible, highlighted by the results of character optimizations indicating that several lineages (e.g. Blaptini in Tenebrioninae) became secondarily adapted to arid environments. These secondary shifts likely occurred multiple times during the evolutionary history of darkling beetles, as several subfamilies encompass xerophilic tribes (two tribes out of nine in Lagriinae; 11 tribes out of 29 in Tenebrioninae and five tribes out of 11 in Diaperinae).Figure 2


Cretaceous environmental changes led to high extinction rates in a hyperdiverse beetle family.

Kergoat GJ, Bouchard P, Clamens AL, Abbate JL, Jourdan H, Jabbour-Zahab R, Genson G, Soldati L, Condamine FL - BMC Evol. Biol. (2014)

Maximum likelihood character trait optimization of habitat preferences. Ancestral character states that are significantly supported are highlighted using either an orange label (for “arid/semi-arid” habitat preferences) or a green label (for “other” habitat preferences). Grey labels indicate ancestral characters for which the difference in log-likelihood is lower than 2.0. For each genus, information on systematics is provided using abbreviated subfamilial and tribal names. A picture of a typical xerophilic species (Onymacris rugatipennis) is also included.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4210489&req=5

Fig2: Maximum likelihood character trait optimization of habitat preferences. Ancestral character states that are significantly supported are highlighted using either an orange label (for “arid/semi-arid” habitat preferences) or a green label (for “other” habitat preferences). Grey labels indicate ancestral characters for which the difference in log-likelihood is lower than 2.0. For each genus, information on systematics is provided using abbreviated subfamilial and tribal names. A picture of a typical xerophilic species (Onymacris rugatipennis) is also included.
Mentions: Contrary to the arid-dwelling Pimeliinae, the other subfamilies are currently more diverse in tropical environments (see Matthews et al. [25] for details). Thus if we consider that phylogenetic biome conservatism holds in many groups [32], this suggests that distinct tenebrionid lineages were already adapted to arid or tropical environments before the end of the KTR. Results from character optimization analyses support this hypothesis and suggest that the common ancestor of tenebrionid beetles was adapted to arid environments (Figure 2). Arid environments were extremely widespread in the Early Jurassic [33,34]; though they progressively receded with the break-up of the Pangaea [6,7], they never completely disappeared, which could explain the persistence of distinct lineages of pimeliine beetles across eastern and western hemispheres [25]. Interestingly, pimeliine beetles are currently nearly absent from Australia, where aridification began in the Miocene and deserts only appeared very recently [35,36]. As underlined by Matthews et al. [25], this suggests that the group was strictly adapted to arid environments from the beginning, and unable to colonize the Australian continent before its isolation in the middle of the Cenozoic. The only exceptions are the few representatives (nine species) of two plesiotypic tribes (Cnemeplatiini and Vacronini) that were possibly present as coastal sand dune inhabitants before separation from Gondwana [37]. Other groups such as the rain-forest specialists Adeliini [29] originated about 96 Ma (median age of 95.13 Ma, 95% HPD: 82.69-113.95 Ma), possibly in the warm temperate forests that were widespread in the southern hemisphere at that time [4]. This is also the case for other tropical groups in the subfamily Tenebrioninae (tribes Heleini and Titaeini), whose most recent common ancestor diversified at the beginning of the Late Cretaceous, around 100 Ma (median age of 99.83 Ma, 95% HPD: 91.76-111.76 Ma). In some of these groups the phylogenetic biome conservatism is not irreversible, highlighted by the results of character optimizations indicating that several lineages (e.g. Blaptini in Tenebrioninae) became secondarily adapted to arid environments. These secondary shifts likely occurred multiple times during the evolutionary history of darkling beetles, as several subfamilies encompass xerophilic tribes (two tribes out of nine in Lagriinae; 11 tribes out of 29 in Tenebrioninae and five tribes out of 11 in Diaperinae).Figure 2

Bottom Line: As attested by the fossil record, Cretaceous environmental changes have significantly impacted the diversification dynamics of several groups of organisms.Contrary to other insect groups, we found no support for a positive shift in diversification rates during the Cretaceous; instead there is evidence for an 8.5-fold increase in extinction rates that was not compensated by a joint increase in speciation rates.We hypothesize that this pattern is better explained by the concomitant reduction of arid environments starting in the mid-Cretaceous, which likely negatively impacted the diversification of arid-adapted species that were predominant at that time.

View Article: PubMed Central - PubMed

Affiliation: INRA - UMR 1062 CBGP (INRA, IRD, CIRAD, Montpellier SupAgro), Campus de Baillarguet, Montferrier-sur-Lez, 34988, France. kergoat@supagro.inra.fr.

ABSTRACT

Background: As attested by the fossil record, Cretaceous environmental changes have significantly impacted the diversification dynamics of several groups of organisms. A major biome turnover that occurred during this period was the rise of angiosperms starting ca. 125 million years ago. Though there is evidence that the latter promoted the diversification of phytophagous insects, the response of other insect groups to Cretaceous environmental changes is still largely unknown. To gain novel insights on this issue, we assess the diversification dynamics of a hyperdiverse family of detritivorous beetles (Tenebrionidae) using molecular dating and diversification analyses.

Results: Age estimates reveal an origin after the Triassic-Jurassic mass extinction (older than previously thought), followed by the diversification of major lineages during Pangaean and Gondwanan breakups. Dating analyses indicate that arid-adapted species diversified early, while most of the lineages that are adapted to more humid conditions diversified much later. Contrary to other insect groups, we found no support for a positive shift in diversification rates during the Cretaceous; instead there is evidence for an 8.5-fold increase in extinction rates that was not compensated by a joint increase in speciation rates.

Conclusions: We hypothesize that this pattern is better explained by the concomitant reduction of arid environments starting in the mid-Cretaceous, which likely negatively impacted the diversification of arid-adapted species that were predominant at that time.

Show MeSH
Related in: MedlinePlus