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Evolutionary shifts in extant mustelid (Mustelidae: Carnivora) cranial shape, body size and body shape coincide with the Mid-Miocene Climate Transition

DOI:10.1098/rsbl.2019.0155
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Chris J Law at University of Texas at Austin
Chris J Law
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Abstract

Environmental changes can lead to evolutionary shifts in phenotypic traits, which in turn facilitate the exploitation of novel adaptive landscapes and lineage diversification. The global cooling, increased aridity and expansion of open grasslands during the past 50 Myr are prime examples of new adaptive landscapes that spurred lineage and ecomorphological diversity of several mammalian lineages such as rodents and large herbivorous megafauna. However, whether these environmental changes facilitated evolutionary shifts in small- to mid-sized predator morphology is unknown. Here, I used a complete cranial and body morphological dataset to examine the timing of evolutionary shifts in cranial shape, body size and body shape within extant mustelids (martens, otters, polecats and weasels) during the climatic and environmental changes of the Cenozoic. I found that evolutionary shifts in all three traits occurred within extant mustelid subclades just after the onset of the Mid-Miocene Climate Transition. These mustelid subclades first shifted towards more elongate body plans followed by concurrent shifts towards smaller body sizes and more robust crania. I hypothesize that these cranial and body morphological shifts enabled mustelids to exploit novel adaptive zones associated with the climatic and environmental changes of the Mid to Late Miocene, which facilitated significant increases in clade carrying capacity.
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Research
Cite this article: Law CJ. 2019 Evolutionary
shifts in extant mustelid (Mustelidae:
Carnivora) cranial shape, body size and body
shape coincide with the Mid-Miocene Climate
Transition. Biol. Lett. 15: 20190155.
http://dx.doi.org/10.1098/rsbl.2019.0155
Received: 1 March 2019
Accepted: 8 May 2019
Subject Areas:
evolution
Keywords:
body elongation, diversification, ecological
opportunity, morphological innovation,
Musteloidea, trait evolution
Author for correspondence:
Chris J. Law
e-mail: cjlaw@ucsc.edu
Electronic supplementary material is available
online at https://dx.doi.org/10.6084/m9.
figshare.c.4507244.
Evolutionary biology
Evolutionary shifts in extant mustelid
(Mustelidae: Carnivora) cranial shape,
body size and body shape coincide with
the Mid-Miocene Climate Transition
Chris J. Law
Ecology and Evolutionary Biology, University of California Santa Cruz, 130 McAllister Way, Santa Cruz,
CA 95060, USA
CJL, 0000-0003-1575-7746
Environmental changes can lead to evolutionary shifts in phenotypic traits,
which in turn facilitate the exploitation of novel adaptive landscapes and
lineage diversification. The global cooling, increased aridity and expansion
of open grasslands during the past 50 Myr are prime examples of new
adaptive landscapes that spurred lineage and ecomorphological diversity
of several mammalian lineages such as rodents and large herbivorous
megafauna. However, whether these environmental changes facilitated
evolutionary shifts in small- to mid-sized predator morphology is unknown.
Here, I used a complete cranial and body morphological dataset to examine
the timing of evolutionary shifts in cranial shape, body size and body shape
within extant mustelids (martens, otters, polecats and weasels) during the
climatic and environmental changes of the Cenozoic. I found that evolution-
ary shifts in all three traits occurred within extant mustelid subclades just
after the onset of the Mid-Miocene Climate Transition. These mustelid
subclades first shifted towards more elongate body plans followed by
concurrent shifts towards smaller body sizes and more robust crania.
I hypothesize that these cranial and body morphological shifts enabled
mustelids to exploit novel adaptive zones associated with the climatic and
environmental changes of the Mid to Late Miocene, which facilitated
significant increases in clade carrying capacity.
1. Introduction
The exceptional lineage and phenotypic diversity found across the tree of life is
often associated with increases in ecological opportunities through the evolution
of innovations, extinction of competitors or environmental changes [1– 3]. Simpson
[1] was one of the first to recognize that the adaptive landscapes of phenotypic traits
can shift ( jump) in response to environmental changes. The global cooling,
increased aridity and habitat shift from forest to grasslands during the past
50 Myr [4– 7] is a prime exampleofenvironmental changes that spurred evolution-
ary shifts in phenotypes. Several mammalian clades have adapted to these
environmental transitions towards more open, grass-dominated habitats. Rodents
and lagomorphs diversified and shifted towards increased tooth crown height
(i.e. hypsodonty) to eat tougher grass material and evolved adaptations for more
efficient burrowing, jumping and cursorial locomotion across the open habitats
(reviewed in [8]). Herbivorous ungulates also shifted towards hypsodont dentition
during the Oligocene to Miocene, along with the lengthening of limbs for more effi-
cient cursoriality during the late Miocene [9–12]. Similarly, ecomorphological
diversity of carnivores increased [13–15], with large carnivores shifting from
ambush specialists to active pursuit specialists during the late Miocene to
&2019 The Author(s) Published by the Royal Society. All rights reserved.
... Therefore, we observed larger individuals in the water that most likely overcame the physiological restrictions imposed by this habitat, in spite of their exclusively carnivorous habit (Fig. 3d). Despite body size of predators and prey being positively correlated in some groups (Shine, 1991;Portalier et al., 2018), a previous study revealed that abiotic constraints were crucial on evolutionary shifts in mustelids body plan (Law, 2019), that allowed them to explore new environments for resources (see below; King & Powell, 2006). One of these modifications was the broader cranial shape and large jaw muscles, which compensate for their small bodies allowing them to consume prey up to 10 times larger than their own body mass (Law, 2019). ...
... Despite body size of predators and prey being positively correlated in some groups (Shine, 1991;Portalier et al., 2018), a previous study revealed that abiotic constraints were crucial on evolutionary shifts in mustelids body plan (Law, 2019), that allowed them to explore new environments for resources (see below; King & Powell, 2006). One of these modifications was the broader cranial shape and large jaw muscles, which compensate for their small bodies allowing them to consume prey up to 10 times larger than their own body mass (Law, 2019). As a consequence, these morphological innovations may have hampered body size evolution driven by item consumption from specific trophic guilds, although aspects of the diet may have contributed to the evolution of body shape rather than size. ...
... Why? This heat loss can be offset by the extreme efficiency of these predators in hunting prey, which allows them to enter burrows and crevices, precisely because of their body shape (Brown & Lasiewski, 1972) and changes associated with the skull, which increased their efficiency as predators (Law, 2019). These evolutive modifications as response to open habitat expansions and prey diversification (Law, 2019) provided the energy input necessary to supply the high losses and were triggered by very strong selection pressures towards this specific shape. ...
Habitat Drives Body Size Evolution in Mustelidae (Mammalia: Carnivora)
Article
Full-text available
Body size of organisms is often associated with physiological demands and habitat structure. Several theories and models have been proposed to explain body size trends across geographical space and evolutionary time. It is proposed that herbivores are larger due to their more voluminous digestive system, allowing a longer retention time of the digested material. Simultaneously, for carnivores, it is expected that the bigger the prey, the larger the predator. Additionally, some body size trends have been attributed to climatic variation across space and habitat structure. Bergmann’s Rule proposes that larger endotherms inhabit colder areas, once a larger body size promotes better heat retention due to reduced surface/volume ratio. Similarly, aquatic endotherms are larger than expected, due to analogous physiological demands to endotherms living in colder environments. Here we tested whether body size of the Mustelidae clade can be explained by diet, habitat structure or environmental temperature. We performed phylogenetic regressions to assess the relationships between body size and the aforementioned predictors in 53 species of Mustelidae. We found that neither diet nor temperature were related to body size evolution. However, habitat was related to body size, with semi aquatic species being larger. Mechanisms involving thermal inertia, predation pressure, better quality resources close to water and bone density are hypotheses that suggest larger body sizes evolution in semi-aquatic vertebrates. We highlight the importance of considering widely accepted ecological traits for large groups, at lower taxonomic levels, in order to expand our understanding of the maintenance of these standards on different scales.
View
... Therefore, we observed larger individuals 201 in the water that most likely overcame the physiological restrictions imposed by this habitat, in spite of their 202 exclusively carnivorous habit (Fig 3d). Despite body size of predators and prey being positively correlated in some 203 groups (Shine, 1991;Portlaier et al., 2018), a previous study revealed that abiotic constraints were crucial on 204 evolutionary shifts in mustelids body plan (Law, 2019), that allowed them to explore new environments for 205 resources (see below; King and Powell, 2006). One of these modifications was the broader cranial shape and large 206 jaw muscles, which compensate for their small bodies allowing them to consume prey up to 10 times larger than 207 their own body mass (Law, 2019). ...
... Despite body size of predators and prey being positively correlated in some 203 groups (Shine, 1991;Portlaier et al., 2018), a previous study revealed that abiotic constraints were crucial on 204 evolutionary shifts in mustelids body plan (Law, 2019), that allowed them to explore new environments for 205 resources (see below; King and Powell, 2006). One of these modifications was the broader cranial shape and large 206 jaw muscles, which compensate for their small bodies allowing them to consume prey up to 10 times larger than 207 their own body mass (Law, 2019). As a consequence, these morphological innovations may have hampered body 208 6 size evolution driven by item consumption from specific trophic guilds, although aspects of the diet may have 209 contributed to the evolution of body shape rather than size. ...
... Why? This heat loss can be offset by the extreme efficiency 226 of these predators in hunting prey, which allows them to enter burrows and crevices, precisely because of their 227 body shape (Brown & Lasiewski, 1972) and changes associated with the skull, which increased their efficiency 228 as predators (Law, 2019). These evolutive modifications as response to open habitat expansions and prey 229 diversification (Law, 2019) provided the energy input necessary to supply the high losses and were triggered by 230 very strong selection pressures towards this specific shape. ...
Habitat drives body size evolution in Mustelidae (Mammalia: Carnivora)
Preprint
Full-text available
  • Oct 2022
Body size of organisms is often associated with physiological demands and habitat structure. Several theories and models have been proposed to explain body size trends across geographical space and evolutionary time. It is proposed that herbivores are larger due to their more voluminous digestive system, allowing a longer retention time of the digested material. Simultaneously, for carnivores, it is expected that the bigger the prey, the larger the predator. Additionally, some body size trends have been attributed to climatic variation across space and habitat structure. Bergmann's Rule proposes that larger endotherms inhabit colder areas, once a larger body size promotes better heat retention due to reduced surface/volume ratio. Similarly, aquatic endotherms are larger than expected, due to analogous physiological demands to endotherms living in colder environments. Here we tested whether body size of the Mustelidae clade can be explained by diet, habitat structure or environmental temperature. We performed phylogenetic regressions to assess the relationships between body size and the aforementioned predictors in 53 species of Mustelidae. We found that neither diet nor temperature were related to body size evolution. However, habitat was related to body size, with semi aquatic species being. Mechanisms involving thermal inertia, predation pressure, better quality resources close to water and bone density are hypotheses that suggest larger body sizes evolution in semi-aquatic vertebrates. We highlight the importance of considering widely accepted ecological traits for large groups, at lower taxonomic levels, in order to expand our understanding of the maintenance of these standards on different scales.
View
... For example, the 'grasslands-associated' subclade contains viruses and paleoviruses that infect (or infected) phylogenetically distinct host species groups that share grassland habitat. It includes equine infectious anaemia virus (EIAV) which infects horses, and two ERV lineages -RELIK (found in leporids) and MELV (found in mustelids) [42][43][44]. Notably, the grassland adaptation of these three host species groups took place in a similar time-period (early-to-middle Miocene) in interconnected biogeographic areas (Laurasia and Africa) [42][43][44] (Fig. 2), suggesting that the connections between the viruses in this clade could re ect inter-order transmission events that took place in a shared habitat. ...
... It includes equine infectious anaemia virus (EIAV) which infects horses, and two ERV lineages -RELIK (found in leporids) and MELV (found in mustelids) [42][43][44]. Notably, the grassland adaptation of these three host species groups took place in a similar time-period (early-to-middle Miocene) in interconnected biogeographic areas (Laurasia and Africa) [42][43][44] (Fig. 2), suggesting that the connections between the viruses in this clade could re ect inter-order transmission events that took place in a shared habitat. ...
An endogenous lentivirus in the germline of a rodent
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  • Sep 2022
Lentiviruses (genus Lentivirus ) are complex retroviruses that infect a broad range of mammals, including humans. Unlike many other retrovirus genera, lentiviruses have only rarely been incorporated into the mammalian germline. However, a small number of endogenous retrovirus (ERV) lineages have been identified, and these rare genomic “fossils” can provide crucial insights into the long-term history of lentivirus evolution. Here, we describe a previously unreported endogenous lentivirus lineage in the genome of the South African springhare ( Pedetes capensis ), demonstrating that the host range of lentiviruses has historically extended to rodents (order Rodentia). Furthermore, through comparative and phylogenetic analysis of lentivirus and ERV genomes, considering the biogeographic and ecological characteristics of host species, we reveal broader insights into the long-term evolutionary history of the genus.
View
... For example, the 20 'grasslands-associated' subclade contains viruses and paleoviruses that infect (or infected) 21 phylogenetically distinct host species groups that share grassland habitat. It includes equine 22 infectious anaemia virus (EIAV) which infects horses, and two ERV lineages -RELIK (found 23 in leporids) and MELV (found in mustelids) [42][43][44]. Notably, the grassland adaptation of 24 these three host species groups took place in a similar time-period (early-to-middle Miocene) 25 ...
... in interconnected biogeographic areas (Laurasia and Africa) [42][43][44] (Fig. 2), suggesting that 26 the connections between the viruses in this clade could reflect inter-order transmission 27 events that took place in a shared habitat. 28 . ...
An endogenous lentivirus in the germline of a rodent
Preprint
Full-text available
  • Sep 2022
Lentiviruses (genus Lentivirus) are complex retroviruses that infect a broad range of mammals, including humans. Unlike many other retrovirus genera, lentiviruses have only rarely been incorporated into the mammalian germline. However, a small number of endogenous retrovirus (ERV) lineages have been identified, and these rare genomic "fossils" can provide crucial insights into the long-term history of lentivirus evolution. Here, we describe a previously unreported endogenous lentivirus lineage in the genome of the South African springhare (Pedetes capensis), demonstrating that the host range of lentiviruses has historically extended to rodents (order Rodentia). Furthermore, through comparative and phylogenetic analysis of lentivirus and ERV genomes, considering the biogeographic and ecological characteristics of host species, we reveal broader insights into the long-term evolutionary history of the genus.
View
... The Early Pleistocene and the rapid climate changes triggered the disappearance of many large carnivores or limited their biodiversity in North China (Farjand, 2020). However, Mustelidae demonstrates an excellent ability to adjust themselves to these palaeoecological changes (Law, 2019). The presence of Eirictis in North and East China and simultaneously in the lower latitudes of South China is a testimony to their resilience. ...
View
... biogeographic distribution. It could potentially be significant that the diverse mammalian groups in which lentiviruses of the 'grassland-associated' clade are found (horses, bovids, mustelids and felids-see Fig. 1) all adapted to a grassland habitat during this period, in interconnected biogeographic areas (Laurasia and Africa) [36][37][38] (Fig. 2). Regarding the ultimate origins of lentiviruses in mammals, molecular clock-based analyses of DELV insertions supports the presence of archaeolentiviruses in Asia (the only region where colugos occur) up to 60 Mya [26] -i.e., throughout most of the Cenozoic Era. ...
An endogenous lentivirus in the germline of a rodent
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Full-text available
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View
... Indeed, although the precise number of taxonomic bursts is still debated, several authors have hypotheses that the unique ecological and morphological diversity observed within mustelids species [63][64][65][66] are the result of an adaptive radiation event 67,68 . Moreover, some mustelids species (in particular the node including the Helictindinae, Guloninae, Ictonychinae, Mustelinae and Lutrinae subfamilies) experienced a diversification in their body shape during the Mid-Miocene Climate Transition which coincides with the significant change in the rate of evolution of the relative brain size revealed by our analyses 69 . Surprisingly, the shift in diversification rate for the skull shape identified by Law 69 appears to be a subsequent event to the diversification of the relative brain size revealed by our analyses, meaning that cranial shape did not constrain the relative brain evolution for these species. ...
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The reasons why some animals have developed larger brains has long been a subject of debate. Yet, it remains unclear which selective pressures may favour the encephalization and how it may act during evolution at different taxonomic scales. Here we studied the patterns and tempo of brain evolution within the order Carnivora and present large-scale comparative analysis of the effect of ecological, environmental, social, and physiological variables on relative brain size in a sample of 174 extant carnivoran species. We found a complex pattern of brain size change between carnivoran families with differences in both the rate and diversity of encephalization. Our findings suggest that during carnivorans' evolution, a trade-off have occurred between the cognitive advantages of acquiring a relatively large brain allowing to adapt to specific environments, and the metabolic costs of the brain which may constitute a disadvantage when facing the need to colonize new environments.
View
... I stress that this result should not be taken to mean that body mass evolution is not adaptive in carnivorans, nor that selection on body mass may not be strong and directional over microevolutionary timescales (Hereford et al., 2004;Kingsolver et al., 2001;Kingsolver & Pfennig, 2004;Schluter, 1988); but see Rollinson & Rowe 2015). Rather, despite the importance of body mass for many aspects of organismal ecology, microevolutionary patterns need not scale to macroevolutionary levels (Jablonski, 1996), and adaptive peaks associated with body size variation are likely not stable at geographic (Diniz-Filho & Tôrres, 2002;Diniz-Filho et al., 2009;Roycroft et al., 2020) or temporal scales ranging from seasonal (Powell & King, 1997) to geologic (Finarelli, 2007;Law, 2019;Slater, 2015). ...
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Inference of Adaptive Shifts for Multivariate Correlated Traits
Article
To study the evolution of several quantitative traits, the classical phylogenetic comparative framework consists of a multivariate random process running along the branches of a phylogenetic tree. The Ornstein-Uhlenbeck (OU) process is sometimes preferred to the simple Brownian Motion (BM) as it models stabilizing selection toward an optimum. The optimum for each trait is likely to be changing over the long periods of time spanned by large modern phylogenies. Our goal is to automatically detect the position of these shifts on a phylogenetic tree, while accounting for correlations between traits, which might exist because of structural or evolutionary constraints. We show that, in the presence of shifts, phylogenetic Principal Component Analysis (pPCA) fails to decorrelate traits efficiently, so that any method aiming at finding shifts needs to deal with correlation simultaneously. We introduce here a simplification of the full multivariate OU model, named scalar OU (scOU), which allows for noncausal correlations and is still computationally tractable. We extend the equivalence between the OU and a BM on a re-scaled tree to our multivariate framework. We describe an Expectation Maximization algorithm that allows for a maximum likelihood estimation of the shift positions, associated with a new model selection criterion, accounting for the identifiability issues for the shift localization on the tree. The method, freely available as an R-package (PhylogeneticEM) is fast, and can deal with missing values. We demonstrate its efficiency and accuracy compared to another state-of-the-art method (l1ou) on a wide range of simulated scenarios, and use this new framework to re-analyze recently gathered datasets on New World Monkeys and Anolis lizards.
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